Structural stabilization of honeybee wings based on heterogeneous stiffness.

Structural stabilization for a membrane structure under high-frequency vibration is still a recognized problem. In nature, honeybee wings with non-uniform material properties demonstrate excellent anti-interference ability. However, the correlation between the structural stabilization and mechanical properties of insect wings has not been completely verified. Here we demonstrate that the sclerotization diversity partially distinguishes the stiffness inhomogeneity of the wing structure. Furthermore, a wing cross-section model with diversity in elastic modulus is constructed to analyze the effect of stiffness distribution on stress optimization during flight. Our results demonstrate that the heterogeneous stiffness promotes the stress distribution and structural stabilization of the wing during flight, which may inspire more optimal designs for anisotropic high-strength membrane structures.

Mechanism of elastic energy storage of honey bee abdominal muscles under stress relaxation.

Energy storage of passive muscles plays an important part in frequent activities of honey bee abdomens due to the muscle distribution and open circulatory system. However, the elastic energy and mechanical properties of structure in passive muscles remain unclear. In this article, stress relaxation tests on passive muscles from the terga of the honey bee abdomens were performed under different concentrations of blebbistatin and motion parameters. In stress relaxation, the load drop with the rapid and slow stages depending on stretching velocity and stretching length reflects the features of myosin-titin series structure and cross-bridge-actin cyclic connections in muscles. Then a model with 2 parallel modules based on the 2 feature structures in muscles was thus developed. The model described the stress relaxation and stretching of passive muscles from honey bee abdomen well for a good fitting in stress relaxation and verification in loading process. In addition, the stiffness change of cross-bridge under different concentrations of blebbistatin is obtained from the model. We derived the elastic deformation of cross-bridge and the partial derivatives of energy expressions on motion parameters from this model, which accorded the experimental results. This model reveals the mechanism of passive muscles from honey bee abdomens suggesting that the temporary energy storage of cross-bridge in terga muscles under abdomen bending provides potential energy for springback during the periodic abdomen bending of honey bee or other arthropod insects. The finding also provides an experimental and theoretical basis for the novel microstructure and material design of bionic muscle.

Physiological Signatures of Changes in Honeybee's Central Complex During Wing Flapping.

Many kinds of locomotion abilities of insects-including flight control, spatial orientation memory, position memory, angle information integration, and polarized light guidance are considered to be related to the central complex. However, evidence was still not sufficient to support those conclusions from the aspect of neural basis. For the locomotion form of wing flapping, little is known about the patterns of changes in brain activity of the central complex during movement. Here, we analyze the changes in honeybees' neuronal population firing activity of central complex and optic lobes with the perspectives of energy and nonlinear changes. Although the specific function of the central complex remains unknown, evidence suggests that its neural activities change remarkably during wing flapping and its delta rhythm is dominative. Together, our data reveal that the firing activity of some of the neuronal populations of the optic lobe shows reduction in complexity during wing flapping. Elucidating the brain activity changes during a flapping period of insects promotes our understanding of the neuro-mechanisms of insect locomotor control, thus can inspire the fine control of insect cyborgs.

Drinking made easier: honey bee tongues dip faster into warmer and/or less viscous artificial nectar.

Optimal concentrations for nectar drinking are limited by the steep increase in the viscosity of sugar solutions with concentration. However, nectar viscosity is inversely related to temperature, which suggests there are advantages to foraging from flowers that are warmer than the surrounding air. The honey bee (Apis mellifera L.) dips nectar using a hairy tongue. However, the microscopic dynamics of the tongue while the bee ingests nectar of varying concentration, viscosity and temperature are unknown. In this study, we found that honey bees respond to the variation of nectar properties by regulating dipping frequency. Through high-speed imaging, we discovered that the honey bee traps warmer sucrose solutions with a quicker tongue. The honey bee dips the warmest and most dilute solution (40°C and 25% w/w sucrose) 1.57 times as fast as the coldest and thickest solution (20°C and 45% w/w sucrose). When the viscosity of different sucrose concentrations was kept constant by adding the inert polysaccharide Tylose, honey bees dipped nectar at constant frequency. We propose a fluid mechanism model to elucidate potential effects on sucrose intake and show that higher dipping frequency can increase the volumetric and energetic intake rates by 125% and 15%, respectively. Our findings broaden insights into how honey bees adapt to foraging constraints from the perspective of tongue dynamics, and demonstrate that elevated intrafloral temperatures and lower nectar viscosity can improve the volumetric and energetic intake rates of pollinators.

Temporal model of fluid-feeding mechanisms in a long proboscid orchid bee compared to the short proboscid honey bee.

Bees (Apidae) are flower-visiting insects that possess highly efficient mouthparts for the ingestion of nectar and other sucrose fluids. Their mouthparts are composed of mandibles and a tube-like proboscis. The proboscis forms a food canal, which encompasses a protrusible and hairy tongue to load and imbibe nectar, representing a fluid-feeding technique with a low Reynolds number. The western honey bee, Apis mellifera ligustica, can rhythmically erect the tongue microtrichia to regulate the glossal shape, achieving a tradeoff between nectar intake rate and viscous drag. Neotropical orchid bees (Euglossa imperialis) possess a proboscis longer than the body and combines this lapping-sucking mode of fluid-feeding with suction feeding. This additional technique of nectar uptake may have different biophysics. In order to reveal the effect of special structures of mouthparts in terms of feeding efficiency, we build a temporal model for orchid bees considering fluid transport in multi-states including active suction, tongue protraction and viscous dipping. Our model indicates that the dipping technique employed by honey bees can contribute to more than seven times the volumetric and energetic intake rate at a certain nectar concentration compared with the combined mode used by orchid bees. The high capability of the honey bee's proboscis to ingest nectar may inspire micropumps for transporting viscous liquid with higher efficiency.

Parallel Mechanism Composed of Abdominal Cuticles and Muscles Simulates the Complex and Diverse Movements of Honey Bee (Apis mellifera L.) Abdomen.

The abdominal intersegmental structures allow insects, such as honey bees, dragonflies, butterflies, and drosophilae, to complete diverse behavioral movements. In order to reveal how the complex abdominal movements of these insects are produced, we use the honey bee (Apis mellifera L.) as a typical insect to study the relationship between intersegmental structures and abdominal motions. Microstructure observational experiments are performed by using the stereoscope and the scanning electron microscope. We find that a parallel mechanism, composed of abdominal cuticle and muscles between the adjacent segments, produces the complex and diverse movements of the honey bee abdomen. These properties regulate multiple behavioral activities such as waggle dance and flight attitude adjustment. The experimental results demonstrate that it is the joint efforts of the muscles and membranes that connected the adjacent cuticles together. The honey bee abdomen can be waggled, expanded, contracted, and flexed with the actions of the muscles. From the view point of mechanics, a parallel mechanism is evolved from the intersegmental connection structures of the honey bee abdomen. Here, we conduct a kinematic analysis of the parallel mechanism to simulate the intersegmental abdominal motions.

A quick tongue: older honey bees dip nectar faster to compensate for mouthpart structure deterioration.

The western honey bee, Apis mellifera L. (Hymenoptera), is arguably the most important pollinator worldwide. While feeding, A. mellifera uses a rapid back-and-forth motion with its brush-like mouthparts to probe pools and films of nectar. Because of the physical forces experienced by the mouthparts during the feeding process, we hypothesized that the mouthparts acquire wear or damage over time, which is paradoxical, because it is the older worker bees that are tasked with foraging for nectar and pollen. Here, we show that the average length of the setae (brush-like structures) on the glossa decreases with honey bee age, particularly when feeding on high-viscosity sucrose solutions. The nectar intake rate, however, remains nearly constant regardless of age or setae length (0.39±0.03 µg s-1 for honey bees fed a 45% sucrose solution and 0.48±0.05 µg s-1 for those fed a 35% sucrose solution). Observations of the feeding process with high-speed video recording revealed that the older honey bees with shorter setae dip nectar at a higher frequency. We propose a liquid transport model to calculate the nectar intake rate, energy intake rate and the power to overcome viscous drag. Theoretical analysis indicates that A. mellifera with shorter glossal setae can compensate both nectar and energy intake rates by increasing dipping frequency. The altered feeding behavior provides insight into how A. mellifera, and perhaps other insects with similar feeding mechanisms, can maintain a consistent fluid uptake rate, despite having damaged mouthparts.

Locking of the operculum in a water snail: Theoretical modeling and applications for mechanical sealing.

How can a water snail lock its door by an operculum? In this theoretical and experimental combined research, we revealed this by dissection, modeling and validation with a 3D printed technique. The operculum is a corneous or calcareous trapdoor-like sheet which attaches to the upper surface of the water snail's foot. It can plug the shell aperture by retracting the soft body when a predator or environmental threat is encountered. For a water snail (Pomacea canaliculata), the operculum can be locked in its shell rapidly. By optical microscope images, we found the operculum of P. canaliculata is a multilayered disk with a thicker center and thinner edge, which may be functionally influential for successful closing and opening the trapdoor. We filmed the locking in opercula of living snails, and designed an experiment to measure the deformation of opercula on the dead samples. We propose one mathematical model to describe the connections among geometry, sectionalized stiffness and the force for locking. By using 3D printing technique, we designed an operculum inspired locking mechanism to validate the theories we proposed. Under the same normal force, the water leakage rate of the bio-inspired structure can be reduced to 99% compared to the disk with uniform thickness. Our results reveal that the snail's operculum not only develops a light-weight trapdoor, but a locking mechanism which could serve as a valuable model for designing compliant locking mechanisms.

Kinematics of Stewart Platform Explains Three-Dimensional Movement of Honeybee's Abdominal Structure.

The Stewart platform is a typical parallel mechanism, used extensively in flight simulators with six degrees of freedom. It is rarely found in animals and has never been reported to regulate and control physiological activities. Now an equivalent Stewart platform structure is found in the honey bee (Hymenoptera: Apidae: Apis mellifera L.) abdomen to explain its three-dimensional movements. The stereoscope and scanning electron microscope are used to observe the internal structures of honeybees' abdomens. Experimental observations show that the muscles and intersegmental membranes connect the terga with the sterna and guarantee the honey bee abdominal movements. From the perspective of mechanics, a Stewart platform is evolved from the lateral connection structure of the honey bee abdomen, and the intrasegmental muscles between the sternum and tergum function as actuators between planes of the Stewart platform. The extraordinary structure provides various advantages for a honey bee to complete a variety of physiological activities. This equivalent Stewart platform structure can also be used to illustrate the flexible abdominal movements of other insects with the segmental abdomen.

Honeybees Prefer to Steer on a Smooth Wall With Tetrapod Gaits.

Insects are well equipped in walking on complex three-dimensional terrain, allowing them to overcome obstacles or catch prey. However, the gait transition for insects steering on a wall remains unexplored. Here, we find that honeybees adopted a tetrapod gait to change direction when climbing a wall. On the contrary to the common tripod gait, honeybees propel their body forward by synchronously stepping with both middle legs and then both front legs. This process ensures the angle of the central axis of the honeybee to be consistent with the crawling direction. Interestingly, when running in an alternating tripod gait, the central axis of honeybee sways around the center of mass under alternating tripod gait to maintain stability. Experimental results show that tripod, tetrapod, and random gaits result in the amazing consensus harmony on the climbing speed and gait stability, whether climbing on a smooth wall or walking on smooth ground.

A Comparative Study of Four Kinds of Adaptive Decomposition Algorithms and Their Applications.

The adaptive decomposition algorithm is a powerful tool for signal analysis, because it can decompose signals into several narrow-band components, which is advantageous to quantitatively evaluate signal characteristics. In this paper, we present a comparative study of four kinds of adaptive decomposition algorithms, including some algorithms deriving from empirical mode decomposition (EMD), empirical wavelet transform (EWT), variational mode decomposition (VMD) and Vold⁻Kalman filter order tracking (VKF_OT). Their principles, advantages and disadvantages, and improvements and applications to signal analyses in dynamic analysis of mechanical system and machinery fault diagnosis are showed. Examples are provided to illustrate important influence performance factors and improvements of these algorithms. Finally, we summarize applicable scopes, inapplicable scopes and some further works of these methods in respect of precise filters and rough filters. It is hoped that the paper can provide a valuable reference for application and improvement of these methods in signal processing.

Drag Reduction in a Natural High-Frequency Swinging Micro-Articulation: Mouthparts of the Honey Bee.

Worker-bee mouthparts consist of the glossa, the galeae and the vestigial labial palp, and it is these structures that enable bees to feed themselves. The articulation joints, 60∼70 µm in diameter, are present on the tip of the labial palp and are covered with olfactory sensilla, allowing movements between the segments. Using a specially designed high-speed camera system, we discovered that the articulation joint could swing in the nectar at a frequency of ∼50 Hz, considerably higher than the usual motion frequency of mammalian joints. To understand the potential drag reduction in this tiny organ, we examined its microstructure and also its surface wettability. We found that chitinous semispherical protuberances (4∼6 µm in diameter) are uniformly scattered on the surface of the joint and, moreover, that the surface is hydrophobic. We proposed a hydrodynamic model and revealed that the specialized surface can effectively reduce the mean equivalent friction (Ff) by ∼10%, through the use of protuberances immersed in the liquid feed. Theoretical results indicated that the dimensions of such protuberances are the predominant factor in minimizing Ff, and that the natural dimensions of the protuberances are close to the theoretical optimum at which friction is at a minimum. These discoveries may inspire the design of high-frequency micro-joints for engineering applications, such as in micro-stirrers.

Drag reduction effects facilitated by microridges inside the mouthparts of honeybee workers and drones.

The mouthpart of a honeybee is a natural well-designed micropump that uses a reciprocating glossa through a temporary tube comprising a pair of galeae and labial palpi for loading nectar. The shapes and sizes of mouthparts differ among castes of honeybees, but the diversities of the functional microstructures inside the mouthparts of honeybee workers and drones remain poorly understood. Through scanning electron microscopy, we found the dimensional difference of uniformly distributed microridges on the inner galeae walls of Apis mellifera ligustica workers and drones. Subsequently, we recorded the feeding process of live honeybees by using a specially designed high-speed camera system. Considering the microridges and kinematics of the glossa, we constructed a hydrodynamic model to calculate the friction coefficient of the mouthpart. In addition, we test the drag reduction through the dimensional variations of the microridges on the inner walls of mouthparts. Theoretical estimations of the friction coefficient with respect to dipping frequency show that inner microridges can reduce friction during the feeding process of honeybees. The effects of drag reduction regulated by specific microridges were then compared. The friction coefficients of the workers and drones were found to be 0.011±0.007 (mean±s.d.) and 0.045±0.010, respectively. These results indicate that the mouthparts of workers are more capable of drag reduction compared with those of drones. The difference was analyzed by comparing the foraging behavior of the workers and drones. Workers are equipped with well-developed hypopharyngeal, and their dipping frequency is higher than that of drones. Our research establishes a critical link between microridge dimensions and drag reduction capability during the nectar feeding of honeybees. Our results reveal that microridges inside the mouthparts of honeybee workers and drones reflect the caste-related life cycles of honeybees.

Critical Structure for Telescopic Movement of Honey bee (Insecta: Apidae) Abdomen: Folded Intersegmental Membrane.

The folded intersegmental membrane is a structure that interconnects two adjacent abdominal segments; this structure is distributed in the segments of the honey bee abdomen. The morphology of the folded intersegmental membrane has already been documented. However, the ultrastructure of the intersegmental membrane and its assistive role in the telescopic movements of the honey bee abdomen are poorly understood. To explore the morphology and ultrastructure of the folded intersegmental membrane in the honey bee abdomen, frozen sections were analyzed under a scanning electron microscope. The intersegmental membrane between two adjacent terga has a Z-S configuration that greatly influences the daily physical activities of the honey bee abdomen. The dorsal intersegmental membrane is 2 times thicker than the ventral one, leading to asymmetric abdominal motion. Honey bee abdominal movements were recorded using a high-speed camera and through phase-contrast computed tomography. These movements conformed to the structural features of the folded intersegmental membrane.

Erection pattern and section-wise wettability of honeybee glossal hairs in nectar feeding.

The honeybee's tongue (glossa) is covered with bushy hairs and resembles a mop or a brush. We examined the dimensions of glossal hairs of the Italian honeybee (Apis mellifera ligustica) and found that the average length of hairs increased from the proximal segment to the distal end. The glossal dynamic surface of a honeybee in drinking cycles was captured by a specially designed high-speed camera system, and we discovered that the glossal hairs erected rhythmically when drinking nectar; specifically, hairs on the proximal segment erected earlier than those on the distal end of a honeybee's tongue, which was identified as the phenomenon of asynchronous hair erection. Moreover, by measuring the wettability of the tongue, we found that the flabellum was the most hydrophilic and the root of the tongue was hardest to be wetted. According to our observations, we suggest that the honeybee has an optimal hair-erection pattern that could balance nectar intake and viscous drag. These results will be helpful to understand the liquid-feeding mechanism of honeybees, especially the role of erectable glossal hairs.

Erection mechanism of glossal hairs during honeybee feeding.

Many animals use their mouthparts or tongue to feed themselves rapidly and efficiently. Honeybees have evolved specialized tongues to collect nectar from flowers. Nectar-intake movements consist of rapid protraction and retraction of glossa from a tube formed by the maxillae and labial palps. We establish a physical model to reveal the driving mechanism of hair erection. Results indicate that the glossa of honeybees is similar to a compression spring. Experimental results show that hair erection is generated by the tension of hyaline rod and the elasticity of segmental sheath. The retractor muscle of hyaline rod is contracted at first, which compresses the sheath of pigmented rings and flattens the hairs. While the retractor muscle of hyaline rod relaxes, the elastic energy storage in the compressed glossal sheath will release to change the equivalent stiffness of glossal sheath and erect glossal hairs. These results explain the erection mechanism of glossal hairs during honeybee feeding.

Switchable Wettability of the Honeybee's Tongue Surface Regulated by Erectable Glossal Hairs.

Various nectarivorous animals apply bushy-hair-equipped tongues to lap nectar from nectaries of flowers. A typical example is provided by the Italian honeybee (Apis mellifera ligustica), who protracts and retracts its tongue (glossa) through a temporary tube, and actively controls the erectable glossal hairs to load nectar. We first examined the microstructure of the honeybee's glossal surface, recorded the kinematics of its glossal hairs during nectar feeding process and observed the rhythmical hair erection pattern clearly. Then we measured the wettability of the glossal surface under different erection angles (EA) in sugar water of the mass concentration from 25 to 45%, mimicked by elongating the glossa specimens. The results show that the EA in retraction approximately remains stable under different nectar concentrations. In a specific concentration (35, 45, or 55%), the contact angle decreases and glossal surface area increases while the EA of glossal hairs rises, the glossa therefore could dynamically alter the glossal surface and wettability in foraging activities, not only reducing the energy consumption for impelling the nectar during tongue protraction, but also improving the nectar-trapping volume for feeding during glossa retraction. The dynamic glossal surface with switchable wettability regulated by erectable hairs may reveal the effective adaptation of the honeybee to nectar intake activities.

Movement Analysis of Flexion and Extension of Honeybee Abdomen Based on an Adaptive Segmented Structure.

Honeybees (Apis mellifera) curl their abdomens for daily rhythmic activities. Prior to determining this fact, people have concluded that honeybees could curl their abdomen casually. However, an intriguing but less studied feature is the possible unidirectional abdominal deformation in free-flying honeybees. A high-speed video camera was used to capture the curling and to analyze the changes in the arc length of the honeybee abdomen not only in free-flying mode but also in the fixed sample. Frozen sections and environment scanning electron microscope were used to investigate the microstructure and motion principle of honeybee abdomen and to explore the physical structure restricting its curling. An adaptive segmented structure, especially the folded intersegmental membrane (FIM), plays a dominant role in the flexion and extension of the abdomen. The structural features of FIM were utilized to mimic and exhibit movement restriction on honeybee abdomen. Combining experimental analysis and theoretical demonstration, a unidirectional bending mechanism of honeybee abdomen was revealed. Through this finding, a new perspective for aerospace vehicle design can be imitated.

Structure Design and Heat Transfer Performance Analysis of a Novel Composite Phase Change Active Cooling Channel Wall for Hypersonic Aircraft.

Efficient and stable heat dissipation structure is crucial for improving the convective heat transfer performance of thermal protection systems (TPSs) for hypersonic aircraft. However, the heat dissipation wall of the current TPS is limited by a single material and structure, inefficiently dissipating the large amount of accumulated heat generated during the high-speed maneuvering flight of hypersonic aircraft. Here, a convection cooling channel structure of TPS is proposed, which is an innovative multi-level structure inspired by the natural honeycomb. An active cooling channel (PCM-HC) is designed by using a variable-density topology optimization method and filled with phase change material (PCM). Numerical simulations are used to investigate the thermal performance of the PCM-HC wall, focusing on the influence of PCM properties, structural geometric parameters, and PCM types on heat transfer characteristics. The results demonstrate that the honeycomb-like convection cooling channel wall, combined with PCM latent heat of phase change, exhibits superior heat dissipation capability. With a heat flux input of 50 kW/m2, the maximum temperature on the inner wall of PCM-HC is reduced by 12 K to 20 K. Different PCMs have opposing effects on heat transfer performance due to their distinct thermophysical properties. This work can provide a theoretical basis for the design of high-efficiency cooling channel, improving the heat dissipation performance in the TPS of hypersonic aircraft.

Excitation of the abdominal ganglion affects the electrophysiological activity of indirect flight muscles of the honeybee Apis mellifera.

Our understanding of the nervous tissues that affect the wing flapping of insects mainly focuses on the brain, but wing flapping is a rhythmic movement related to the central pattern generator in the ventral nerve cord. To verify whether the neural activity of the abdominal ganglion of the honeybee (Apis mellifera) affects the flapping-wing flight, we profiled the response characteristics of indirect flight muscles to abdominal ganglion excitation. Strikingly, a change in the neural activity of ganglion 3 or ganglion 4 has a stronger effect on the electrophysiological activity of indirect flight muscles than that of ganglion 5. The electrophysiological activity of vertical indirect flight muscles is affected more by the change in neural activity of the abdominal ganglion than that of lateral indirect flight muscles. Moreover, the change in neural activity of the abdominal ganglion mainly causes the change in the muscular activity of indirect wing muscles, but the activity patterns change relatively little and there is little change in the complicated details. This work improves our understanding of the neuroregulatory mechanisms associated with the flapping-wing flight of honeybees.