The spider cuticle: a remarkable material toolbox for functional diversity.

Engineered systems are typically based on a large variety of materials differing in composition and processing to provide the desired functionality. Nature, however, has evolved materials that are used for a wide range of functional challenges with minimal compositional changes. The exoskeletal cuticle of spiders, as well as of other arthropods such as insects and crustaceans, is based on a combination of chitin, protein, water and small amounts of organic cross-linkers or minerals. Spiders use it to obtain mechanical support structures and lever systems for locomotion, protection from adverse environmental influences, tools for piercing, cutting and interlocking, auxiliary structures for the transmission and filtering of sensory information, structural colours, transparent lenses for light manipulation and more. This paper illustrates the 'design space' of a single type of composite with varying internal architecture and its remarkable capability to serve a diversity of functions. This article is part of the theme issue 'Bio-derived and bioinspired sustainable advanced materials for emerging technologies (part 1)'.

Einstein, von Frisch and the honeybee: a historical letter comes to light.

The work of the Nobel Laureate Karl von Frisch, the founder of this journal, was seminal in many ways. He established the honeybee as a key animal model for experimental behavioural studies on sensory perception, learning and memory, and first correctly interpreted its famous dance communication. Here, we report on a previously unknown letter by the Physicist and Nobel Laureate Albert Einstein that was written in October 1949. It briefly addresses the work of von Frisch and also queries how understanding animal perception and navigation may lead to innovations in physics. We discuss records proving that Einstein and von Frisch met in April 1949 when von Frisch visited the USA to present a lecture on bees at Princeton University. In the historical context of Einstein's theories and thought experiments, we discuss some more recent discoveries of animal sensory capabilities alien to us humans and potentially valuable for bio-inspired design improvements. We also address the orientation of animals like migratory birds mentioned by Einstein 70 years ago, which pushes the boundaries of our understanding nature, both its biology and physics.

Measuring strain in the exoskeleton of spiders-virtues and caveats.

The measurement of cuticular strain during locomotion using foil strain gauges provides information both on the loads of the exoskeleton bears and the adaptive value of the specific location of natural strain detectors (slit sense organs). Here, we critically review available literature. In tethered animals, by applying loads to the metatarsus tip, strain and mechanical sensitivity (S = strain/load) induced at various sites in the tibia were determined. The loci of the lyriform organs close to the tibia-metatarsus joint did not stand out by high strain. The strains induced at various sites during free locomotion can be interpreted based on S and, beyond the joint region, on beam theory. Spiders avoided laterad loading of the tibia-metatarsus joint during slow locomotion. Balancing body weight, joint flexors caused compressive strain at the posterior and dorsal tibia. While climbing upside down strain measurements indicate strong flexor activity. In future studies, a precise calculation and quantitative determination of strain at the sites of the lyriform organs will profit from more detailed data on the overall strain distribution, morphology, and material properties. The values and caveats of the strain gauge technology, the only one applicable to freely moving spiders, are discussed.

A spider in motion: facets of sensory guidance.

Spiders show a broad range of motions in addition to walking and running with their eight coordinated legs taking them towards their resources and away from danger. The usefulness of all these motions depends on the ability to control and adjust them to changing environmental conditions. A remarkable wealth of sensory receptors guarantees the necessary guidance. Many facets of such guidance have emerged from neuroethological research on the wandering spider Cupiennius salei and its allies, although sensori-motor control was not the main focus of this work. The present review may serve as a springboard for future studies aiming towards a more complete understanding of the spider's control of its different types of motion. Among the topics shortly addressed are the involvement of lyriform slit sensilla in path integration, muscle reflexes in the walking legs, the monitoring of joint movement, the neuromuscular control of body raising, the generation of vibratory courtship signals, the sensory guidance of the jump to flying prey and the triggering of spiderling dispersal behavior. Finally, the interaction of sensors on different legs in oriented turning behavior and that of the sensory systems for substrate vibration and medium flow are addressed.

Mechanics to pre-process information for the fine tuning of mechanoreceptors.

Non-nervous auxiliary structures play a significant role in sensory biology. They filter the stimulus and transform it in a way that fits the animal's needs, thereby contributing to the avoidance of the central nervous system's overload with meaningless stimuli and a corresponding processing task. The present review deals with mechanoreceptors mainly of invertebrates and some remarkable recent findings stressing the role of mechanics as an important source of sensor adaptedness, outstanding performance, and diversity. Instead of organizing the review along the types of stimulus energy (force) taken up by the sensors, processes associated with a few basic and seemingly simple mechanical principles like lever systems, viscoelasticity, resonance, traveling waves, and impedance matching are taken as the guideline. As will be seen, nature makes surprisingly competent use of such "simple mechanics".

Nano-channels in the spider fang for the transport of Zn ions to cross-link His-rich proteins pre-deposited in the cuticle matrix.

We identify the presence of multiple vascular channels within the spider fang. These channels seem to serve the transport of zinc to the tip of the fang to cross-link the protein matrix by binding to histidine residues. According to amino acid and elemental analysis of fangs extracted shortly after ecdysis, His-rich proteins are deposited before Zn is incorporated into the cuticle. Microscopic and spectroscopic investigations in the electron microscope and synchrotron radiation experiments suggest that Zn ions are transported through these channels in a liable (yet unidentified) form, and then form stable complexes upon His binding. The resulting cross-linking through the Zn-His complexes is conferring hardness to the fang. Our observations of nano-channels serving the Zn-transport within the His-rich protein matrix of the fibre reinforced spider fang may also support recent bio-inspired attempts to design artificial polymeric vascular materials for self-healing and in-situ curing.

Stingless bees (Meliponini): senses and behavior.

Stingless bees (Hymenoptera, Apidae, Meliponini) are by far the largest group of eusocial bees on Earth. Due to the diversity of evolutionary responses to specific ecological challenges, the Meliponini are well suited for comparative studies of the various adaptations to the environment found in highly eusocial bees. Of particular interest are the physiological mechanisms underlying the sophisticated cooperative and collective actions of entire colonies, which form the basis of the ecological success of the different bee species under the particular conditions prevailing in their respective environment. The present Special Issue of the Journal of Comparative Physiology A provides a sample of the exciting diversity of sensorial and behavioral adaptations in stingless bees, particularly concerning (1) the sensory bases for foraging, (2) chemical communication, and (3) the behavioral ecology of foraging.

Nectar profitability, not empty honey stores, stimulate recruitment and foraging in Melipona scutellaris (Apidae, Meliponini).

In stingless bees (Meliponini) like in many other eusocial insect colonies food hoarding plays an important role in colony survival. However, very little is known on how Meliponini, a taxon restricted to tropical and subtropical regions, respond to different store conditions. We studied the impact of honey removal on nectar foraging activity and recruitment behaviour in Melipona scutellaris and compared our results with studies of the honey bee Apis mellifera. As expected, foraging activity increased significantly during abundance of artificial nectar and when increasing its profitability. Foraging activity on colony level could thereby frequently increase by an order of magnitude. Intriguingly, however, poor honey store conditions did not induce increased nectar foraging or recruitment activity. We discuss possible reasons explaining why increasing recruitment and foraging activity are not used by meliponines to compensate for poor food conditions in the nest. Among these are meliponine specific adaptations to climatic and environmental conditions, as well as physiology and brood rearing, such as mass provisioning of the brood.

Micromechanical properties of strain-sensitive lyriform organs of a wandering spider (Cupiennius salei).

UNLABELLED: Highly sensitive lyriform organs located on the legs of the wandering spider Cupiennius salei allow the spider to detect nanometer-scale strains in the exoskeleton resulting from locomotion or substrate vibrations. Morphological features of the lyriform organs result in their specialization and selective sensitivity to specific mechanical stimuli, which make them interesting for bioinspired strain sensors. Here we utilize atomic force microscopy (AFM)-based force spectroscopy to probe nano-scale mechanical properties of the covering membrane of two lyriform organs found on Cupiennius salei: the vibration sensitive metatarsal lyriform organ (HS10) and the proprioreceptive tibial lyriform organ (HS8). Force distance curves (FDCs) obtained from AFM measurements displayed characteristic multi-layer structure behavior, with calculated elastic moduli ranging from 150MPa to 500MPa for different regions and indentation depths. In addition, we probed the lyriform organs with a large radius tip, which allowed for probing structural deformation by the application of high forces and large scale deformations without damaging the surface. The viscoelastic behavior of the sensor materials observed in this probing suggests mechanical relaxation times potentially playing a role in the time-dependent behavior of the lyriform organs. STATEMENT OF SIGNIFICANCE: Highly sensitive lyriform organs located on the legs of the wandering spider Cupiennius salei allow the spider to detect nanometer-scale strains in the exoskeleton resulting from locomotion or substrate vibrations. Morphological features of the lyriform organs result in their specialization and selective sensitivity to specific mechanical stimuli, which make them an interesting for bioinspired strain sensors. Here we utilize atomic force microscopy (AFM)-based force spectroscopy to probe nano-scale mechanical properties of the covering membrane of two lyriform organs found on Cupiennius salei: the vibration sensitive metatarsal lyriform organ (HS10) and the proprioreceptive tibial lyriform organ (HS8). Force distance curves (FDCs) obtained from AFM measurements displayed characteristic multi-layer structure behavior, with calculated elastic moduli ranging from 150MPa to 500MPa for different regions and indentation depths. The viscoelastic behavior of the sensor materials observed in this probing suggests mechanical relaxation times playing a role in the time-dependent behavior of the lyriform organs.

Ordering of protein and water molecules at their interfaces with chitin nano-crystals.

Synchrotron X-ray diffraction was applied to study the structure of biogenic α-chitin crystals composing the tendon of the spider Cupiennius salei. Measurements were carried out on pristine chitin crystals stabilized by proteins and water, as well as after their deproteinization and dehydration. We found substantial shifts (up to Δq/q=9% in the wave vector in q-space) in the (020) diffraction peak position between intact and purified chitin samples. However, chitin lattice parameters extracted from the set of reflections (hkl), which did not contain the (020)-reflection, showed no systematic variation between the pristine and the processed samples. The observed shifts in the (020) peak position are discussed in terms of the ordering-induced modulation of the protein and water electron density near the surface of the ultra-thin chitin fibrils due to strong protein/chitin and water/chitin interactions. The extracted modulation periods can be used as a quantitative parameter characterizing the interaction length.

Micro- and nano-structural details of a spider's filter for substrate vibrations: relevance for low-frequency signal transmission.

The metatarsal lyriform organ of the Central American wandering spider Cupiennius salei is its most sensitive vibration detector. It is able to sense a wide range of vibration stimuli over four orders of magnitude in frequency between at least as low as 0.1 Hz and several kilohertz. Transmission of the vibrations to the slit organ is controlled by a cuticular pad in front of it. While the mechanism of high-frequency stimulus transfer (above ca 40 Hz) is well understood and related to the viscoelastic properties of the pad's epicuticle, it is not yet clear how low-frequency stimuli (less than 40 Hz) are transmitted. Here, we study how the pad material affects the pad's mechanical properties and thus its role in the transfer of the stimulus, using a variety of experimental techniques, such as X-ray micro-computed tomography for three-dimensional imaging, X-ray scattering for structural analysis, and atomic force microscopy and scanning electron microscopy for surface imaging. The mechanical properties were investigated using scanning acoustic microscopy and nanoindentation. We show that large tarsal deflections cause large deformation in the distal highly hydrated part of the pad. Beyond this region, a sclerotized region serves as a supporting frame which resists the deformation and is displaced to push against the slits, with displacement values considerably scaled down to only a few micrometres. Unravelling the structural arrangement in such specialized structures may provide conceptual ideas for the design of new materials capable of controlling a technical sensor's specificity and selectivity, which is so typical of biological sensors.

Spider joint hair sensilla: adaptation to proprioreceptive stimulation.

Adding to previous efforts towards a better understanding of the remarkable diversity of spider mechanosensitive hair sensilla, this study examines hairs of Cupiennius salei most likely serving a proprioreceptive function. At the tibia-metatarsus joint of all walking legs, there are two opposing groups of hairs ventrally on the tibia (20 hairs) and metatarsus (75 hairs), respectively. These hairs deflect each other when the joint flexes during locomotion, reversibly interlocking by microtrichs on their hair shafts. The torque resisting the hair deflection into the direction of natural stimulation is smaller by up to two powers of ten than that for the other directions. The torsional restoring constant S of the hair suspension is about 10(-10) Nm rad(-1) in the preferred direction, up to a hair deflection angle of 30° (mean of natural deflection angles). Joint movements were imposed in ranges and at rates measured in walking spiders and sensory action potentials recorded. Within the natural step frequencies (0.3-3 Hz) the rate of action potentials follows the velocity of hair deflection. All findings point to the morphological, mechanical, and physiological adaptedness of the joint hair sensilla to their proprioreceptive stimulation during locomotion.

A spider's biological vibration filter: micromechanical characteristics of a biomaterial surface.

A strain-sensing lyriform organ (HS-10) found on all of the legs of a Central American wandering spider (Cupiennius salei) detects courtship, prey and predator vibrations transmitted by the plant on which it sits. It has been suggested that the viscoelastic properties of a cuticular pad directly adjacent to the sensory organ contribute to the organ's pronounced high-pass characteristics. Here, we investigate the micromechanical properties of the cuticular pad biomaterial in search of a deeper understanding of its impact on the function of the vibration sensor. These properties are considered to be an effective adaptation for the selective detection of signals for frequencies >40 Hz. Using surface force spectroscopy mapping we determine the elastic modulus of the pad surface over a temperature range of 15-40 °C at various loading frequencies. In the glassy state, the elastic modulus was ~100 MPa, while in the rubbery state the elastic modulus decreased to 20 MPa. These data are analyzed according to the principle of time-temperature superposition to construct a master curve that relates mechanical properties, temperature and stimulus frequencies. By estimating the loss and storage moduli vs. temperature and frequency it was possible to make a direct comparison with electrophysiology experiments, and it was found that the dissipation of energy occurs within a frequency window whose position is controlled by environmental temperatures.

Multiscale structural gradients enhance the biomechanical functionality of the spider fang.

The spider fang is a natural injection needle, hierarchically built from a complex composite material comprising multiscale architectural gradients. Considering its biomechanical function, the spider fang has to sustain significant mechanical loads. Here we apply experiment-based structural modelling of the fang, followed by analytical mechanical description and Finite-Element simulations, the results of which indicate that the naturally evolved fang architecture results in highly adapted effective structural stiffness and damage resilience. The analysis methods and physical insights of this work are potentially important for investigating and understanding the architecture and structural motifs of sharp-edge biological elements such as stingers, teeth, claws and more.

Airflow elicits a spider's jump towards airborne prey. II. Flow characteristics guiding behaviour.

When hungry, the wandering spider Cupiennius salei is frequently seen to catch flying insect prey. The success of its remarkable prey-capture jump from its sitting plant into the air obviously depends on proper timing and sensory guidance. In this study, it is shown that particular features of the airflow generated by the insect suffice to guide the spider. Vision and the reception of substrate vibrations and airborne sound are not needed. The behavioural reactions of blinded spiders were examined by exposing them to natural and synthetic flows imitating the fly-generated flow or particular features of it. Thus, the different roles of the three phases previously identified in the fly-generated flow and described in the companion paper could be demonstrated. When exposing the spider to phase I flow only (exponentially increasing flow velocity with very little fluctuation and typical of the fly's approach), an orienting behaviour could be observed but a prey-capture jump never be elicited. Remarkably, the spider reacted to the onset of phase II (highly fluctuating flow) of a synthetically generated flow field with a jump as frequently as it did when exposed to natural fly-generated flows. In all cases using either natural or artificial flows, the spider's jump was triggered before its flow sensors were hit by phase III flow (steadily decreasing airflow velocity). Phase III may tell the spider that the prey has passed by already in case of no prey-capture reaction. Our study underlines the relevance of airflow in spider behaviour. It also reflects the sophisticated workings of their flow sensors (trichobothria) previously studied in detail. Presumably, the information contained in prey-generated airflows plays a similar role in many other arthropods.

Airflow elicits a spider's jump towards airborne prey. I. Airflow around a flying blowfly.

The hunting spider Cupiennius salei uses airflow generated by flying insects for the guidance of its prey-capture jump. We investigated the velocity field of the airflow generated by a freely flying blowfly close to the flow sensors on the spider's legs. It shows three characteristic phases (I-III). (I) When approaching, the blowfly induces an airflow signal near the spider with only little fluctuation (0.013 ± 0.006 m s(-1)) and a strength that increases nearly exponentially with time (maximum: 0.164 ± 0.051 m s(-1) s.d.). The spider detects this flow while the fly is still 38.4 ± 5.6 mm away. The fluctuation of the airflow above the sensors increases linearly up to 0.037 m s(-1) with the fly's altitude. Differences in the time of arrival and intensity of the fly signal at different legs probably inform the spider about the direction to the prey. (II) Phase II abruptly follows phase I with a much higher degree of fluctuation (fluctuation amplitudes: 0.114 ± 0.050 m s(-1)). It starts when the fly is directly above the sensor and corresponds to the time-dependent flow in the wake below and behind the fly. Its onset indicates to the spider that its prey is now within reach and triggers its jump. The spider derives information on the fly's position from the airflow characteristics, enabling it to properly time its jump. The horizontal velocity of the approaching fly is reflected by the time of arrival differences (ranging from 0.038 to 0.108 s) of the flow at different legs and the exponential velocity growth rate (16-79 s(-1)) during phase I. (III) The air flow velocity decays again after the fly has passed the spider.