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.

Model organisms and systems in neuroethology: one hundred years of history and a look into the future.

The Journal of Comparative Physiology lived up to its name in the last 100 years by including more than 1500 different taxa in almost 10,000 publications. Seventeen phyla of the animal kingdom were represented. The honeybee (Apis mellifera) is the taxon with most publications, followed by locust (Locusta migratoria), crayfishes (Cambarus spp.), and fruitfly (Drosophila melanogaster). The representation of species in this journal in the past, thus, differs much from the 13 model systems as named by the National Institutes of Health (USA). We mention major accomplishments of research on species with specific adaptations, specialist animals, for example, the quantitative description of the processes underlying the axon potential in squid (Loligo forbesii) and the isolation of the first receptor channel in the electric eel (Electrophorus electricus) and electric ray (Torpedo spp.). Future neuroethological work should make the recent genetic and technological developments available for specialist animals. There are many research questions left that may be answered with high yield in specialists and some questions that can only be answered in specialists. Moreover, the adaptations of animals that occupy specific ecological niches often lend themselves to biomimetic applications. We go into some depth in explaining our thoughts in the research of motion vision in insects, sound localization in barn owls, and electroreception in weakly electric fish.

A Comparison of Aerodynamic Parameters in Two Subspecies of the American Barn Owl (Tyto furcata).

Aerodynamic parameters, such as wing loading, are important indicators of flight maneuverability. We studied two subspecies of the American Barn owl (Tyto furcata), the North American subspecies, T.f.pratincola, and the Galapagos subspecies, T.f.punctatissima, with respect to aerodynamic parameters and compared our findings with those in other owl and bird species. The body mass of T.f.pratincola is about two times higher than that of T.f.punctatissima. Wing loading between the two subspecies scales allometrically. Wing loading in T.f.pratincola is about 50% higher than in T.f.punctatissima. The scaling of wing length is not statistically different from the prediction for isometric scaling. By contrast, the wing chord in T.f.punctatissima is larger than predicted by isometric scaling, as is the wing area. The scaling of wing loading observed here for T.f.punctatissima differs considerably from the scaling in other owl and bird species as available in the literature. We speculate that the allometric scaling helps T.f.punctatissima to catch smaller prey such, as insects that are found in many pellets of T.f.punctatissima, despite the fact that in both subspecies, small rodents make up most of the diet.

Development of the horizontal optocollic reflex in juvenile barn owls (Tyto furcata pratincola).

Adult barn owls and primates possess an almost symmetric monocular rotational horizontal optocollic reflex. In primates, the reflex is initially asymmetric and becomes symmetric with time after birth. The condition in barn owls has not been studied so far. Here, we present data on the development of this reflex in this bird. We tested juvenile barn owls from the time before they open their eyes after hatching to the time they reach adult feather length. Wide-field visual patterns served as stimuli. They were presented at different rotational speeds in binocular and monocular settings. The binocular horizontal optocollic responses of juvenile barn owls were symmetric and adult-like on the first day that the birds responded to the stimulus. The monocular responses showed different rates of development in respect to stimulus velocity and stimulus direction. For velocities up to 20 deg/s, the monocular reflex was also adult-like on the first day that the birds responded to the stimulus. An initially higher asymmetry for 30 deg/s compared to adults disappeared within about two weeks. The development at even higher velocities remained unclear.

Optocollic responses in adult barn owls (Tyto furcata).

Barn owls, like primates, have frontally oriented eyes, which allow for a large binocular overlap. While owls have similar binocular vision and visual-search strategies as primates, it is less clear whether reflexive visual behavior also resembles that of primates or is more similar to that of closer related, but lateral-eyed bird species. Test cases are visual responses driven by wide-field movement: the optokinetic, optocollic, and optomotor responses, mediated by eye, head and body movements, respectively. Adult primates have a so-called symmetric horizontal response: they show the same following behavior, if the stimulus, presented to one eye only, moves in the nasal-to-temporal direction or in the temporal-to-nasal direction. By contrast, lateral-eyed birds have an asymmetric response, responding better to temporal-to-nasal movement than to nasal-to-temporal movement. We show here that the horizontal optocollic response of adult barn owls is less asymmetric than that in the chicken for all velocities tested. Moreover, the response is symmetric for low velocities (< 20 deg/s), and similar to that of primates. The response becomes moderately asymmetric for middle-range velocities (20-40 deg/s). A definitive statement for the complex situation for higher velocities (> 40 deg/s) is not possible.

Integrity of and damage to wings, feather vanes and serrations in barn owls.

The silent flight of owls is well known. It has served as role model for the designs of new airplane wings and ventilators. One of the structural features that underlies silent flight is the serrated leading edge of the wing that is mainly formed by the tenth primary flight feather (P10). We examined here how much the wings, the P10 feather and the serrations in different populations of barn owls reflect the intact situation. First, when the P10 feather molts, no or fewer serrations are present. Furthermore, damage to feathers and serrations may occur. Damage may be due to several factors like broken feather tips, lost rami, barbules, or broken tips of serrations. The latter may cause a narrowing of the outer vane of the P10 feather. We quantitatively assessed damage by counting the number of wings with missing or broken primary feathers, the number of wings with a narrowed outer vane of the P10 feather, and the number of serrations with reduced length. Considerable damage occurred on wings and feathers on both the macroscopic and microscopic levels. The observed damage most likely influences flight performance. More damage occurred in Galapagos barn owls than in North American and European barn owls. The Galapagos population may be more vulnerable than the other populations because it may at least temporarily be in a bad nutritional state and, thus, postpone molt.

Flow turning effect and laminar control by the 3D curvature of leading edge serrations from owl wing.

This work describes a novel mechanism of laminar flow control of straight and backward swept wings with a comb-like leading edge (LE) device. It is inspired by the LE comb on owl feathers and the special design of its barbs, resembling a cascade of complex 3D-curved thin finlets. The details of the geometry of the barbs from an owl feather were used to design a generic model of the comb for experimental and numerical flow studies with the comb attached to the LE of a flat plate. Due to the owls demonstrating a backward sweep of the wing during gliding and flapping from live recordings, our examinations have also been carried out at differing sweep angles. The results demonstrate a flow turning effect in the boundary layer inboards, which extends downstream in the chordwise direction over distances of multiples of the barb lengths. The inboard flow-turning effect described here, counter-acts the outboard directed cross-span flow typically appearing for backward swept wings. This flow turning behaviour is also shown on SD7003 airfoil using precursory LES investigations. From recent theoretical studies on a swept wing, such a way of turning the flow in the boundary layer is known to attenuate crossflow instabilities and delay transition. A comparison of the comb-induced cross-span velocity profiles with those proven to delay laminar to turbulent transition in theory shows excellent agreement, which supports the laminar flow control hypothesis. Thus, the observed effect is expected to delay transition in owl flight, contributing to a more silent flight.

A cortex-like canonical circuit in the avian forebrain.

Although the avian pallium seems to lack an organization akin to that of the cerebral cortex, birds exhibit extraordinary cognitive skills that are comparable to those of mammals. We analyzed the fiber architecture of the avian pallium with three-dimensional polarized light imaging and subsequently reconstructed local and associative pallial circuits with tracing techniques. We discovered an iteratively repeated, column-like neuronal circuitry across the layer-like nuclear boundaries of the hyperpallium and the sensory dorsal ventricular ridge. These circuits are connected to neighboring columns and, via tangential layer-like connections, to higher associative and motor areas. Our findings indicate that this avian canonical circuitry is similar to its mammalian counterpart and might constitute the structural basis of neuronal computation.

Ear asymmetry in Tengmalm's owl (Aegolius funereus): Two phases of asymmetrical development of the squamoso-occipital wing.

Ear asymmetry is an adaptive characteristic present in the order of owls (Strigiformes). It developed independently up to seven times in this taxon and is accompanied by morphological adaptations in bones or soft tissues around or at the ear openings. Within all strigiform species, the Boreal or Tengmalm's owl (Aegolius funereus) possesses a particularly complex bilateral ear asymmetry that results from modifications of the neurocranium and some cartilaginous elements. While the ear asymmetry in adult birds has been described in detail, data on its development is scarce. Here we describe the development of the asymmetric squamoso-occipital wing of A. funereus from its embryonic origin up to adulthood. The asymmetry of the squamoso-occipital wing develops in two phases. Firstly, it originates as a cartilaginous structure in the last ten days before hatching. Its frontal margin shows a bilateral asymmetry from the beginning of its development while the rostro-ventral process stays symmetrical up to post-hatching day 35. Secondly, when the fledglings have already left the nest, the squamoso-occipital wing ossifies. Moreover, the rostro-ventral process on the right side grows towards the eyeball, while there is no relative displacement on the left side. Thus, the developmental process in A. funereus differs from that in the barn owl that develops its soft tissue asymmetry in one phase and completes the asymmetry before hatching. The new data presented here extend our knowledge of the mechanisms underlying the asymmetric skull development in owls.

Expression patterns of chloride transporters in the auditory brainstem of developing chicken.

GABAergic transmission changes from depolarization to hyperpolarization in most vertebrate brain regions during development. By contrast, in the auditory brainstem of chicken a depolarizing effect of GABA persists after hatching. Since auditory brainstem neurons that receive GABAergic input have a Cl- reversal potential above resting membrane potential, a specifically tuned activity of Cl- transporters is likely. We here present a developmental study of the expression patterns of several members of the SLC12 family (NKCC1, NKCC2, KCC1, KCC2, KCC4, CCC6, CCC9) and of AE3 at developmental ages E7, E10, E12, E15, E17, and P1 with quantitative RT-PCR. NKCC2 and CCC9 were not detected in auditory brainstem (positive control: kidney). KCC1, CCC6 and AE3 were expressed, but not regulated, while NKCC1, KCC2 and KCC4 were regulated. The expression of the latter transporters increased, with KCC2 exhibiting the strongest expression at all time points. Biochemical analysis of the protein expression of NKCC1, KCC2 and KCC4 corroborated the findings on the mRNA level. All three transporters showed a localization at the outer rim of the cells, with NKCC1 and KCC2 expressed in neurons, and KCC4 predominantly in glia. The comparison of the published chloride reversal potential and expression of transporter proteins suggest strong differences in the efficiency of the three transporters. Further, the strong KCC2 expression could reflect a role in the structural development of auditory brainstem synapses that might lead to changes in the physiological properties.

Sound localization in barn owls studied with manipulated head-related transfer functions: beyond broadband interaural time and level differences.

Interaural time and level differences are important cues for sound localization. We wondered whether the broadband information contained in these two cues could fully explain the behavior of barn owls and responses of midbrain neurons in these birds. To tackle this problem, we developed a novel approach based on head-related transfer functions. These filters contain the complete information present at the eardrum. We selected positions in space characterized by equal broadband interaural time and level differences. Stimulation from such positions provides reduced information to the owl. We show that barn owls are able to discriminate between such positions. In many cases, but not all, the owls may have used spectral components of interaural level differences that exceeded the known behavioral resolution and variability for discrimination. Alternatively, the birds may have used template matching. Likewise, neurons in the optic tectum of the barn owl, a nucleus involved in sensorimotor integration, contained more information than is available in the broadband interaural time and level differences. Thus, these data show that more information is available and used by barn owls for sound localization than carried by broadband interaural time and level differences.

TLR7 Controls VSV Replication in CD169+ SCS Macrophages and Associated Viral Neuroinvasion.

Vesicular stomatitis virus (VSV) is an insect-transmitted rhabdovirus that is neurovirulent in mice. Upon peripheral VSV infection, CD169+ subcapsular sinus (SCS) macrophages capture VSV in the lymph, support viral replication, and prevent CNS neuroinvasion. To date, the precise mechanisms controlling VSV infection in SCS macrophages remain incompletely understood. Here, we show that Toll-like receptor-7 (TLR7), the main sensing receptor for VSV, is central in controlling lymph-borne VSV infection. Following VSV skin infection, TLR7-/- mice display significantly less VSV titers in the draining lymph nodes (dLN) and viral replication is attenuated in SCS macrophages. In contrast to effects of TLR7 in impeding VSV replication in the dLN, TLR7-/- mice present elevated viral load in the brain and spinal cord highlighting their susceptibility to VSV neuroinvasion. By generating novel TLR7 floxed mice, we interrogate the impact of cell-specific TLR7 function in anti-viral immunity after VSV skin infection. Our data suggests that TLR7 signaling in SCS macrophages supports VSV replication in these cells, increasing LN infection and may account for the delayed onset of VSV-induced neurovirulence observed in TLR7-/- mice. Overall, we identify TLR7 as a novel and essential host factor that critically controls anti-viral immunity to VSV. Furthermore, the novel mouse model generated in our study will be of valuable importance to shed light on cell-intrinsic TLR7 biology in future studies.

EvoDevo in owl ear asymmetry-The little owl (Athene noctua).

Owls are well adapted to nocturnal hunting. This includes vision tuned to low level light conditions, silent flight, and asymmetrical ears. Asymmetrical ears facilitate sound localization and evolved up to seven times independently in the evolutionary history of owls. However, there are also owl species with a crepuscular or diurnal lifestyle, like the little owl (Athene noctua), that have symmetrical ears as adults. Here we show that a small, but significant ear asymmetry occurs in the embryonic development of little owls, despite the presence of symmetrical ears in adults. In the asymmetric period, the left ear opening is bigger in area than its counterpart on the right. The asymmetry in the little owl occurs in the same stages at which the asymmetry in the barn owl (Tyto furcata) develops, but in the little owl the asymmetry vanishes shortly before hatching. Asymmetries in the size of the ear openings are also found in the adults of other owl species, most of them belonging to the genus Strix. We interpret our finding as an indication of a secondarily evolved diurnal activity in little owls. Further, ear asymmetry might be more deeply rooted in the evolution of owls than previously assumed.

Kocuria tytonicola, new bacteria from the preen glands of American barn owls (Tyto furcata).

Although birds are hosts to a large number of microorganisms, microbes have rarely been found in avian oil glands. Here, we report on two strains of a new bacterial species from the preen oil of American barn owls (Tyto furcata). Phenotypic as well as genotypic methods placed the isolates to the genus Kocuria. Strains are non-fastidious, non-lipophilic Gram-positive cocci and can be unambiguously discriminated from their closest relative Kocuria rhizophila DSM 11926T. In phylogenetic trees, the owl bacteria formed a distinct cluster which was clearly separated from all other known Kocuria species. The same conclusion was drawn from MALDI-TOF MS analyses. Once again, the new bacterial strains were very similar to one another, but exhibited substantial differences when compared to the most closely related species. Besides, the results of the biochemical tests, optimum growth conditions and pigmentation differed from closely related Kocuria spp. Finally, ANIb values of less than 87% provided striking evidence that the isolates recovered from American barn owls represent a hitherto undescribed species, for which we propose the name Kocuria tytonicola sp. nov. The type strain is 489T (DSM 104133T=LMG 29945T, taxonumber TA00340).

Kocuria tytonis sp. nov., isolated from the uropygial gland of an American barn owl (Tyto furcata).

Avian uropygial glands have received increasing attention in recent years, but little is known about micro-organisms in uropygial glands. In this study, we isolated a strain of Gram-stain-positive, non-motile, non-spore-forming cocci, designated 442T, from the uropygial gland of an American barn owl (Tyto furcata) and characterized it using a polyphasic approach. 16S rRNA gene sequence analysis placed the isolate in the genus Kocuria. The G+C content was 70.8 mol%, the major menaquinone was MK-7(H2) and the predominant cellular fatty acids were anteiso-C15 : 0, anteiso-C17 : 0 and iso-C15 : 0. Phylogenetic analyses based on the 16S rRNA gene identified Kocuria rhizophila DSM 11926T (99.6 % similarity), Kocuria salsicia DSM 24776T (98.7 %), Kocuria varians DSM 20033T (98.3 %) and Kocuria marina DSM 16420T (98.3 %) as the most closely related species. However, average nucleotide identity values below 86 % indicated that the isolate differed from all species hitherto described. Chemotaxonomic analyses and whole-cell protein profiles corroborated these findings. Accordingly, the isolate is considered to be a member of a novel species, for which the name Kocuria tytonis sp. nov. is proposed. The type strain is 442T (=DSM 104130T=LMG 29944T).

Behavioral Evidence and Neural Correlates of Perceptual Grouping by Motion in the Barn Owl.

Perceiving an object as salient from its surround often requires a preceding process of grouping the object and background elements as perceptual wholes. In humans, motion homogeneity provides a strong cue for grouping, yet it is unknown to what extent this occurs in nonprimate species. To explore this question, we studied the effects of visual motion homogeneity in barn owls of both genders, at the behavioral as well as the neural level. Our data show that the coherency of the background motion modulates the perceived saliency of the target object. An object moving in an odd direction relative to other objects attracted more attention when the other objects moved homogeneously compared with when moved in a variety of directions. A possible neural correlate of this effect may arise in the population activity of the intermediate/deep layers of the optic tectum. In these layers, the neural responses to a moving element in the receptive field were suppressed when additional elements moved in the surround. However, when the surrounding elements all moved in one direction (homogeneously moving), they induced less suppression of the response compared with nonhomogeneously moving elements. Moreover, neural responses were more sensitive to the homogeneity of the background motion than to motion-direction contrasts between the receptive field and the surround. The findings suggest similar principles of saliency-by-motion in an avian species as in humans and show a locus in the optic tectum where the underlying neural circuitry may exist.SIGNIFICANCE STATEMENT A critical task of the visual system is to arrange incoming visual information to a meaningful scene of objects and background. In humans, elements that move homogeneously are grouped perceptually to form a categorical whole object. We discovered a similar principle in the barn owl's visual system, whereby the homogeneity of the motion of elements in the scene allows perceptually distinguishing an object from its surround. The novel findings of these visual effects in an avian species, which lacks neocortical structure, suggest that our basic visual perception shares more universal principles across species than presently thought, and shed light on possible brain mechanisms for perceptual grouping.

Visual search in barn owls: Task difficulty and saccadic behavior.

How do we find what we are looking for? A target can be in plain view, but it may be detected only after extensive search. During a search we make directed attentional deployments like saccades to segment the scene until we detect the target. Depending on difficulty, the search may be fast with few attentional deployments or slow with many, shorter deployments. Here we study visual search in barn owls by tracking their overt attentional deployments-that is, their head movements-with a camera. We conducted a low-contrast feature search, a high-contrast orientation conjunction search, and a low-contrast orientation conjunction search, each with set sizes varying from 16 to 64 items. The barn owls were able to learn all of these tasks and showed serial search behavior. In a subsequent step, we analyzed how search behavior of owls changes with search complexity. We compared the search mechanisms in these three serial searches with results from pop-out searches our group had reported earlier. Saccade amplitude shortened and fixation duration increased in difficult searches. Also, in conjunction search saccades were guided toward items with shared target features. These data suggest that during visual search, barn owls utilize mechanisms similar to those that humans use.

Response adaptation in the barn owl's auditory space map.

Response adaptation is the change of the firing rate of neurons induced by a preceding stimulus. It can be found in many sensory systems and throughout the auditory pathway. We investigated response adaptation in the external nucleus of the inferior colliculus (ICX) of barn owls ( Tyto furcata), a nocturnal bird of prey and specialist in sound localization. Individual neurons in the ICX represent locations in auditory space by maximally responding to combinations of interaural time and level differences (ITD and ILD). Neuronal responses were recorded extracellularly under ketamine-diazepam anesthesia. Response adaptation was observed in three double stimulation paradigms. In two paradigms, the same binaural parameters for both stimuli were chosen. A variation of the level of the second stimulus yielded a level increase sufficient to compensate for adaptation around 5 dB. Introducing a silent interstimulus interval (ISI) resulted in recovery from adaptation. The time course of recovery was followed by varying the ISI, and full recovery was found after an ISI of 50 ms. In a third paradigm, the ITD of the second stimulus was varied to investigate the representation of ITD under adaptive conditions. We found that adaptation led to an increased precision and improved selectivity while the best ITD was stable. These changes of representation remained for longer ISIs than were needed to recover from response adaptation at the best ITD. Stimuli with non-best ITDs could also induce similar adaptive effects if the neurons responded to these ITDs. NEW & NOTEWORTHY We demonstrate and characterize response adaptation in neurons of the auditory space map in the barn owl's midbrain with acoustic double-stimulation paradigms. An increase of the second level by 5 dB compensated for the observed adaptive effect. Recovery from adaptation was faster than in upstream nuclei of the auditory pathway. Our results also show that response adaptation might improve precision and selectivity in the representation of interaural time difference.

Contribution of action potentials to the extracellular field potential in the nucleus laminaris of barn owl.

Extracellular field potentials (EFP) are widely used to evaluate in vivo neural activity, but identification of multiple sources and their relative contributions is often ambiguous, making the interpretation of the EFP difficult. We have therefore analyzed a model EFP from a simple brainstem circuit with separable pre- and postsynaptic components to determine whether we could isolate its sources. Our previous papers had shown that the barn owl neurophonic largely originates with spikes from input axons and synapses that terminate on the neurons in the nucleus laminaris (NL) (Kuokkanen PT, Wagner H, Ashida G, Carr CE, Kempter R. J Neurophysiol 104: 2274-2290, 2010; Kuokkanen PT, Ashida G, Carr CE, Wagner H, Kempter R. J Neurophysiol 110: 117-130, 2013; McColgan T, Liu J, Kuokkanen PT, Carr CE, Wagner H, Kempter R. eLife 6: e26106, 2017). To determine how much the postsynaptic NL neurons contributed to the neurophonic, we recorded EFP responses in NL in vivo. Power spectral analyses showed that a small spectral component of the evoked response, between 200 and 700 Hz, could be attributed to the NL neurons' spikes, while nucleus magnocellularis (NM) spikes dominate the EFP at frequencies ≳1 kHz. Thus, spikes of NL neurons and NM axons contribute to the EFP in NL in distinct frequency bands. We conclude that if the spectral components of source types are different and if their activities can be selectively modulated, the identification of EFP sources is possible. NEW & NOTEWORTHY Extracellular field potentials (EFPs) generate clinically important signals, but their sources are incompletely understood. As a model, we have analyzed the auditory neurophonic in the barn owl's nucleus laminaris. There the EFP originates predominantly from spiking in the afferent axons, with spectral power ≳1 kHz, while postsynaptic laminaris neurons contribute little. In conclusion, the identification of EFP sources is possible if they have different spectral components and if their activities can be modulated selectively.

Size discrimination in barn owls as compared to humans.

We tested how well barn owls can discriminate objects of different sizes. This ability may be important for the owls when catching prey. We performed a quantitative experiment in the laboratory and trained owls in a task in which the owls had to discriminate whether two rhombi presented simultaneously on a computer monitor were of the same or of different sizes. We obtained full data sets with two experienced owls and one data point with a third owl. For objects being sufficiently larger than the spatial resolution of the barn owl, the angular threshold was related to object size, implying that the discrimination followed Weber's law. The range of Weber fractions we determined was between 0.026 and 0.09. For object sizes close to the spatial resolution, performance degraded. We conducted similar experiments with human subjects. Human thresholds showed the same dependence on object size, albeit down to smaller object sizes. Human performance resulted in a range of Weber fractions extending from 0.025 to 0.036. The differences between owls and humans could be explained by the much higher spatial acuity of humans compared with owls.