Interaction of barn owl leading edge serrations with freestream turbulence.

The silent flight of barn owls is associated with wing and feather specialisations. Three special features are known: a serrated leading edge that is formed by free-standing barb tips which appears as a comb-like structure, a soft dorsal surface, and a fringed trailing edge. We used a model of the leading edge comb with 3D-curved serrations that was designed based on 3D micro-scans of rows of barbs from selected barn-owl feathers. The interaction of the flow with the serrations was measured with Particle-Image-Velocimetry in a flow channel at uniform steady inflow and was compared to the situation of inflow with freestream turbulence, generated from the turbulent wake of a cylinder placed upstream. In steady uniform flow, the serrations caused regular velocity streaks and a flow turning effect. When vortices of different size impacted the serrations, the serrations reduced the flow fluctuations downstream in each case, exemplified by a decreased root-mean-square value of the fluctuations in the wake of the serrations. This attenuation effect was stronger for the spanwise velocity component, leading to an overall flow homogenization. Our findings suggest that the serrations of the barn owl provide a passive flow control leading to reduced leading-edge noise when flying in turbulent environments.

The incomparable fascination of comparative physiology: 40 years with animals in the field and laboratory.

This paper is not meant to be a review article. Instead, it gives an overview of the major research projects that the author, together with his students, colleagues and collaborators, has worked on. Although the main focus of the author's work has always been the fish lateral line, this paper is mainly about all the other research projects he did or that were done in his laboratory. These include studies on fishing spiders, weakly electric fish, seals, water rats, bottom dwelling sharks, freshwater rays, venomous snakes, birds of prey, fire loving beetles and backswimmers. The reasons for this diversity of research projects? Simple. The authors's lifelong enthusiasm for animals, and nature's ingenuity in inventing new biological solutions. Indeed, this most certainly was a principal reason why Karl von Frisch and Alfred Kühn founded the Zeitschrift für vergleichende Physiologie (now Journal of Comparative Physiology A) 100 years ago.

Hydrodynamic reception in the Australian water rat, Hydromys chrysogaster.

The Australian water rat, Hydromys chrysogaster, preys on a wide variety of aquatic and semiaquatic arthropods and vertebrates, including fish. A frequently observed predatory strategy of Hydromys is sitting in wait at the water's edge with parts of its vibrissae submersed. Here we show that Hydromys can detect water motions with its whiskers. Behavioural thresholds range from 1.0 to 9.4 mm s-1 water velocity, based on maximal horizontal water velocity in the area covered by the whiskers. This high sensitivity to water motions would enable Hydromys to detect fishes passing by. No responses to surface waves generated by a vibrating rod and resembling the surface waves caused by struggling insects were found.

Stimulus discrimination and surface wave source localization in Crocodilians.

Juvenile Nile crocodiles (Crocodylus niloticus) and spectacled caimans (Caiman crocodilus) use water surface waves for the detection of prey, usually insects trapped at the water surface. This prey detection relies on mechanosensors, the integumentary sensory organs. We found by go/no go conditioning that C. niloticus and C. crocodilus can discriminate surface waves that differ in frequency. On average, frequency difference thresholds were about 4-5 %, e.g. C. niloticus and C. crocodilus distinguished a 40 Hz surface wave from a 38,5 Hz surface wave stimulus. C. niloticus and C. crocodilus also discriminated between single-frequency surface waves (15 Hz or 40 Hz) and surface waves that showed an abrupt frequency change (e.g. from 15 to 16.5 Hz or from 40 Hz to 38.5 Hz). The threshold for the abrupt frequency changes averaged 3-9 %. Additionally, Nile crocodiles differentiated also between a single-frequency water surface wave and a water surface wave that was amplitude modulated. C. niloticus also determined the direction (mean error angle between 13,7° and 16,6°) to a surface wave stimulus. Furthermore, the distance covered by the Nile crocodiles increased slightly with increasing source distance. This was true whether a single-frequency (15 Hz or 40 Hz, relative distance error between 36 and 37%) or a multi-frequency (band width 1 - 80 Hz, relative distance error 25%) surface wave stimulus was offered. Even if the rewarded stimulus (40 Hz) was superimposed by an unrewarded surface wave some distance determination was observed (relative distance error between 30 and 62%).

Form-function relationship in artificial lateral lines.

We examined the form-function relationship of laboratory-constructed artificial lateral line canals. These biomimetic flow sensors consisted of a transparent silicone bar located inside a fluid filled canal equipped with canal pores. The silicone bar guided the light from a LED towards a position- sensitive photodiode. Fluid motion inside the canal deflected the silicone bar which was detected by the photodiode. We found that the resonance frequency of the silicone bar determined the resonance frequency of the artificial lateral line (frequency at which the sensor was most sensitive). The thickness and length of the silicone bar influenced both, the resonance frequency and the sensitivity (across all tested frequencies) of the artificial lateral line sensor. Sensitivity was also influenced by the length and diameter of the artificial lateral line canals. The distance between canal pores determined the spatial resolution of the sensor. The functionality of the sensor in detecting oscillatory fluid motions remained when the canal pores were covered with flexible membranes. Tension, diameter and thickness of the membranes altered the temporal filter properties of the artificial lateral line neuromast. The density and viscosity of the fluid inside the artificial lateral line canals also influenced the sensitivity and temporal filter properties of the artificial lateral line. The acquired knowledge will allow us to optimize artificial lateral line systems for specific technical applications.

A new bioinspired method for pressure and flow sensing based on the underwater air-retaining surface of the backswimmer Notonecta.

In technical systems, static pressure and pressure changes are usually measured with piezoelectric materials or solid membranes. In this paper, we suggest a new biomimetic principle based on thin air layers that can be used to measure underwater pressure changes. Submerged backswimmers (Notonecta sp.) are well known for their ability to retain air layers on the surface of their forewings (hemelytra). While analyzing the hemelytra of Notonecta, we found that the air layer on the hemelytra, in combination with various types of mechanosensitive hairs (clubs and pins), most likely serve a sensory function. We suggest that this predatory aquatic insect can detect pressure changes and water movements by sensing volume changes of the air layer under water. In the present study, we used a variety of microscopy techniques to investigate the fine structure of the hemelytra. Furthermore, we provide a biomimetic proof of principle to validate our hypothesis. The suggested sensory principle has never been documented before and is not only of interest for sensory biologists but can also be used for the development of highly sensitive underwater acoustic or seismographic sensory systems.

The peregrine falcon's rapid dive: on the adaptedness of the arm skeleton and shoulder girdle.

During a dive, peregrine falcons (Falco peregrinus) can reach a velocity of up to 320 km h- 1. Our computational fluid dynamics simulations show that the forces that pull on the wings of a diving peregrine can reach up to three times the falcon's body mass at a stoop velocity of 80 m s- 1 (288 km h- 1). Since the bones of the wings and the shoulder girdle of a diving peregrine falcon experience large mechanical forces, we investigated these bones. For comparison, we also investigated the corresponding bones in European kestrels (Falco tinnunculus), sparrow hawks (Accipiter nisus) and pigeons (Columba livia domestica). The normalized bone mass of the entire arm skeleton and the shoulder girdle (coracoid, scapula, furcula) was significantly higher in F. peregrinus than in the other three species investigated. The midshaft cross section of the humerus of F. peregrinus had the highest second moment of area. The mineral densities of the humerus, radius, ulna, and sternum were highest in F. peregrinus, indicating again a larger overall stability of these bones. Furthermore, the bones of the arm and shoulder girdle were strongest in peregrine falcons.

Responses of medullary lateral line units of the rudd, Scardinius erythrophthalmus, and the nase, Chondrostoma nasus, to vortex streets.

Fish use their mechanosensory lateral line amongst others for the detection of vortices shed by an upstream object and/or for the detection of vortices caused by the tail fin movements of another fish. Thus, vortices are one type of hydrodynamic stimuli to which fish are exposed in their natural environment. We investigated the responses of medullary lateral line units of common rudd, Scardinius erythrophthalmus, and common nase, Chondrostoma nasus (Cyprinidae), to water flow (9.5-13.3 cm-1) that contained vortices (a Kármán vortex street) shed by an upstream cylinder (diameter 2 cm). The distance between the cylinder and the tip of the fish's snout varied between 8 and 24 cm. 21 out of 42 units (S. erythrophthalmus), respectively, 9 out of 39 units (Chondrostoma nasus) responded to the vortices shed by the cylinder. Up to a cylinder distance of 24 cm, interburst intervals revealed the vortex shedding frequency, i.e., burst frequency was similar to or identical with the vortex shedding frequency.

The muscle activity of trout exposed to unsteady flow.

In running water trout seek out special regions for station holding. Trout exposed to flow fluctuations caused by a cylinder hold station immediately upstream of the cylinder (bow wake region), adjacent to the cylinder (entraining region) or downstream of the cylinder (Kármán gait). In addition it was shown that the activity of the axial red swimming muscles is reduced during Kármán gaiting. Up to now only the two-dimensional (horizontal) extensions of the above regions have been examined. We determined both, the horizontal and vertical extension of the Kármán gait, entraining and bow wake region by continuously recording the position (spatial resolution 1 cm3) of trout for 3 h. In addition we continuously recorded the trunk muscle activity. The Kármán gate region had the smallest vertical extension (13 cm, water level 28-29 cm, length of the submerged cylinder 27 cm), followed by the entraining (21 cm) and bow wake region (25 cm). A fourth so far unknown region used for station holding was immediately below a stationary surface wave which, at flow velocities ≥36 cm s- 1, developed slightly downstream of the cylinder. While in any of the above regions the activity of the axial swimming muscles was significantly reduced.

Smart Mechanical Dipole: a device for the measurement of sphere motion in behavioral and neurophysiological experiments.

Fluid motion and pressure fields induced by vibrating spheres are frequently used to investigate the function of biological mechanosensory systems and artificial sensors. The calibration of the sphere motion amplitude (displacement, velocity, acceleration), time course and vibration direction often demands expensive equipment. To mitigate this requirement, we have developed a high-quality, low-cost device that we term a 'Smart Mechanical Dipole'. It provides real-time measurement of sphere acceleration along three axes and can be used to obtain an accurate stimulation trace. We applied digital filtering to equalize the frequency response of the vibrating sphere, which also reduced unwanted amplitude and frequency changes in the hydrodynamic signal. In addition, we show that the angular orientation of the rod to which the sphere was attached, i.e. axial versus transverse, but not the immersion depth of the sphere affected sphere vibration behavior.

Responses of infrared-sensitive tectal units of the pit viper Crotalus atrox to moving objects.

Rattlesnakes perceive IR radiation with their pit organs. This enables them to detect and strike towards warm-blooded prey even in the dark. In addition, the IR sense allows rattlesnakes to find places for thermoregulation. Animate objects (e.g., prey) tend to move and thus cause moving IR images across the pit membrane. Even when an object is stationary, scanning head movements of rattlesnakes will result in moving IR images across the pit membrane. We recorded the neuronal activity of IR-sensitive tectal neurons of the rattlesnake Crotalus atrox while stimulating the snakes with an IR source that moved horizontally at various velocities. As long as object velocity was low (angular velocity of ~5°/s) IR-sensitive tectal neurons hardly showed any responses. With increasing object velocity though, neuronal activity reached a maximum at ~50°/s. A further increase in object velocity up to ~120°/s resulted in a slight decrease of neuronal activity. Our results demonstrate the importance of moving stimuli for the snake's IR detection abilities: in contrast to fast moving objects, stationary or slowly moving objects will not be detected when the snake is motionless, but might be detected by scanning head movements.

Crocodylus niloticus (Crocodilia) is highly sensitive to water surface waves.

Crocodiles show oriented responses to water surface wave stimuli but up to now behavioral thresholds are missing. This study determines the behavioral thresholds of crocodilians to water surface waves. Nile crocodiles (Crocodylus niloticus) were conditioned to respond to single-frequency water surface wave stimuli (duration 1150 ms, frequency 15, 30, 40, 60 and 80 Hz), produced by blowing air onto the water surface. Our study shows that C. niloticus is highly sensitive to capillary water surface waves. Threshold values decreased with increasing frequency and ranged between 10.3 µm (15 Hz) and 0.5 µm (80 Hz) peak-to-peak wave amplitude. For the frequencies 15 Hz and 30 Hz the sensitivity of one spectacled caiman (Caiman crocodilus) to water surface waves was also tested. Threshold values were 12.8 µm (15 Hz) down to 1.76 µm (30 Hz), i.e. close to the threshold values of C. niloticus. The surface wave sensitivity of crocodiles is similar to the surface wave sensitivity of semi-aquatic insects and fishing spiders but does not match the sensitivity of surface-feeding fishes which is higher by one to two orders of magnitude.

Medullary lateral line units of rudd, Scardinius erythrophthalmus, are sensitive to Kármán vortex streets.

We investigated the responses of medullary lateral line units of the rudd, Scardinius erythrophthalmus, to bulk water flow (7 cm s(-1)) and to water flow that contained vortices shed by an upstream half cylinder (diameter 1, 2, and 3 cm). Thirty-five percent of the medullary units either increased or decreased their discharge rate with the increasing cylinder diameter. In some units, the spike patterns revealed the vortex shedding frequency, i.e., in these units the amplitude of spike train frequency spectra was similar or identical to the vortex shedding frequency.

µ-Biomimetic flow-sensors--introducing light-guiding PDMS structures into MEMS.

In the area of biomimetics, engineers use inspiration from natural systems to develop technical devices, such as sensors. One example is the lateral line system of fish. It is a mechanoreceptive system consisting of up to several thousand individual sensors called neuromasts, which enable fish to sense prey, predators, or conspecifics. So far, the small size and high sensitivity of the lateral line is unmatched by man-made sensor devices. Here, we describe an artificial lateral line system based on an optical detection principle. We developed artificial canal neuromasts using MEMS technology including thick film techniques. In this work, we describe the MEMS fabrication and characterize a sensor prototype. Our sensor consists of a silicon chip, a housing, and an electronic circuit. We demonstrate the functionality of our µ-biomimetic flow sensor by analyzing its response to constant water flow and flow fluctuations. Furthermore, we discuss the sensor robustness and sensitivity of our sensor and its suitability for industrial and medical applications. In sum, our sensor can be used for many tasks, e.g. for monitoring fluid flow in medical applications, for detecting leakages in tap water systems or for air and gas flow measurements. Finally, our flow sensor can even be used to improve current knowledge about the functional significance of the fish lateral line.

Morphology and frictional properties of scales of Pseudopus apodus (Anguidae, Reptilia).

In the lizard family Anguidae different levels of limb reduction exist up to a completely limbless body. The locomotion patterns of limbless anguid lizards are similar to the undulating and concertina movements of snakes. Additionally, anguid lizards frequently use a third mode of locomotion, called slide-pushing. During slide-pushing the undulating moving body slides on the ground, while the posterior part of the body is pressed against the substrate. Whereas the macroscopic and microscopic adaptations of snake scales to limbless locomotion are well described, the micromorphology of anguid lizard scales has never been examined. Therefore we studied the macro- and micromorphology of the scales of Pseudopus apodus, an anguid lizard with a snakelike body. In addition, we measured the frictional properties of Pseudopus scales. Our data show that the microstructures of the ventral scales of this anguid lizard are less developed than in snakes. We found, however, a rostro-caudal gradient in macroscopic structuring. Whereas the ventral side of the anterior body was nearly unstructured, the tail had macroscopic longitudinal ridges. Our frictional measurements on rough substrates revealed that the ridges provide a frictional anisotropy: friction was higher in the lateral than in the rostral direction. The observed frictional properties are advantageous for a tail-based slide-pushing locomotion, for which a tail with a high lateral friction is most effective in generating propulsion.

Morphological properties of the last primaries, the tail feathers, and the alulae of Accipiter nisus, Columba livia, Falco peregrinus, and Falco tinnunculus.

We investigated the mechanical properties (Young's modulus, bending stiffness, barb separation forces) of the tenth primary of the wings, of the alulae and of the middle tail feathers of Falco peregrinus. For comparison, we also investigated the corresponding feathers in pigeons (Columba livia), kestrels (Falco tinnunculus), and sparrowhawks (Accipiter nisus). In all four species, the Young's moduli of the feathers ranged from 5.9 to 8.4 GPa. The feather shafts of F. peregrinus had the largest cross-sections and the highest specific bending stiffness. When normalized with respect to body mass, the specific bending stiffness of primary number 10 was highest in F. tinnunculus, while that of the alula was highest in A. nisus. In comparison, the specific bending stiffness, measured at the base of the tail feathers and in dorso-ventral bending direction, was much higher in F. peregrinus than in the other three species. This seems to correlate with the flight styles of the birds: F. tinnunculus hovers and its primaries might therefore withstand large mechanical forces. A. nisus has often to change its flight directions during hunting and perhaps needs its alulae for this maneuvers, and in F. peregrinus, the base of the tail feathers might need a high stiffness during breaking after diving.

Microornamentation of leaf chameleons (Chamaeleonidae: Brookesia, Rhampholeon, and Rieppeleon)--with comments on the evolution of microstructures in the Chamaeleonidae.

Chameleons (Chamaeleonidae) feature many adaptations to their arboreal lifestyle, including zygodactylous feet, a prehensile tail, and epidermal microstructures. In arboreal tree chameleons, the substrate-contacting site of the feet and tail is covered by microscopic hair-like structures (setae) of 6-20 µm length. Their friction enhancing function has been shown in recent studies. Leaf chameleons and one representative of the tree chameleons (Chamaeleo namaquensis) secondarily have become ground-dwelling. Because leaf chameleons are paraphyletic, one could expect that in the three leaf chameleon genera Brookesia, Rhampholeon, and Rieppeleon and the tree chameleon Ch. namaquensis, epidermis has adapted independently to terrestrial locomotion. Using scanning electron microscopy, we investigated the substrate-contacting surfaces of the feet (subdigital) of 17 leaf chameleon species and five tree chameleon species that have not yet been examined. Additionally, surfaces not involved in locomotion, the flanks (dorsolateral), and scale interstices, were examined. Although the subdigital microstructures in leaf chameleons are more diverse than in tree chameleons, we found some features across the genera. The subdigital microornamentation of Rhampholeon spinosus consists of long thin setae and spines, comparable to those of tree chameleons. All other Rhampholeon species have spines or short but broad setae. Rh. spectrum had tooth-like structures instead of setae. Subdigital scales of Brookesia have either thorns or conical scale-tops in the center and feature honeycomb microstructures. In Rieppeleon, subdigital scales have a thorn. Scale surfaces are covered by honeycombs and short hair-like structures (spines). As subdigital scales with a thorn in the center and honeycomb microstructures were also found in the terrestrial tree chameleon Ch. namaquensis, one can assume that this geometry is a convergent adaptation to terrestrial locomotion. Despite the great number of genus-specific traits, the convergent evolution of honey-comb structures in Brookesia, Rieppeleon, and Ch. namaquensis and the high variability of spines and setae in Rhampholeon suggests a rapid adaptation of subdigital microornamentation in Chamaeleonidae.

A µ-biomimetic flow sensor for medical and pharmaceutical applications.

Flow sensing is pivotal in many medical and pharmaceutical applications. Most commercial flow sensors are either expensive, complex, or consume a lot of energy, while low cost sensors usually lack sensitivity, robustness, or long-term stability. In addition, the maintenance and sterilization of most commercial flow sensors is difficult to perform. Here, we present a new µ-biomimetic flow sensor based on the fish lateral line. It measures flow velocity and detects the transition between laminar and turbulent flow, thereby fulfilling most requirements for medical and pharmaceutical applications. Additionally, it has a modular setup featuring a screened or passive bypass configuration, enabling it not only to meter flow in medical applications but also under harsh or well-defined environmental conditions, such as found in pharmaceutical applications. The sensor is robust and can be easily cleaned. Individual parts of the sensor can even be replaced or sterilized. In sum, this sensor opens up a whole new field of applications in the area of medical and pharmaceutical related flow monitoring.

Function of lateral line canal morphology.

Fish perceive water motions and pressure gradients with their lateral line. Lateral line information is used for prey detection, spatial orientation, predator avoidance, schooling behavior, intraspecific communication and station holding. The lateral line of most fishes consists of superficial neuromasts (SNs) and canal neuromasts (CNs). The distribution of SNs and CNs shows a high degree of variation among fishes. Researchers have speculated for decades about the functional significance of this diversity, often without any conclusive answers. Klein et al. (2013) examined how tubules, pore number and pore patterns affect the filter properties of lateral line canals in a marine teleost, the black prickleback (Xiphister atropurpureus). A preliminary mathematical model was formulated and biomimetic sensors were built. For the present study the mathematical model was extended to understand the major underlying principle of how canal dimensions influence the filter properties of the lateral line. Both the extended mathematical model and the sensor experiments show that the number and distribution of pores determine the spatial filter properties of the lateral line. In an environment with little hydrodynamic noise, simple and complex lateral line canals have comparable response properties. However, if exposed to highly turbulent conditions, canals with numerous widely spaced pores increase the signal to noise ratio significantly.

The brain creates illusions not just for us: sharks (Chiloscyllium griseum) can "see the magic" as well.

Bamboo sharks (Chiloscyllium griseum) were tested for their ability to perceive subjective and illusionary contours as well as line length illusions. Individuals were first trained to differentiate between squares, triangles, and rhomboids in a series of two alternative forced-choice experiments. Transfer tests then elucidated whether Kanizsa squares and triangles, grating gaps and phase shifted abutting gratings were also perceived and distinguished. The visual systems of most vertebrates and even invertebrates perceive illusionary contours despite the absence of physical luminance, color or textural differences. Sharks are no exception to the rule; all tasks were successfully mastered within 3-24 training sessions, with sharks discriminating between various sets of Kanizsa figures and alternative stimuli, as well as between subjective contours in >75% of all tests. However, in contrast to Kanizsa figures and subjective contours, sharks were not deceived by Müller-Lyer (ML) illusions. Here, two center lines of equal length are comparatively set between two arrowheads or -tails, in which case the line featuring the two arrow tails appears to be longer to most humans, primates and birds. In preparation for this experiment, lines of varying length, and lines of unequal length randomly featuring either two arrowheads or -tails on their ends, were presented first. Both sets of lines were successfully distinguished by most sharks. However, during presentation of the ML illusions sharks failed to succeed and succumbed either to side preferences or chose according to chance.