The respiratory system influences flight mechanics in soaring birds.

The subpectoral diverticulum (SPD) is an extension of the respiratory system in birds that is located between the primary muscles responsible for flapping the wing1,2. Here we survey the pulmonary apparatus in 68 avian species, and show that the SPD was present in virtually all of the soaring taxa investigated but absent in non-soarers. We find that this structure evolved independently with soaring flight at least seven times, which indicates that the diverticulum might have a functional and adaptive relationship with this flight style. Using the soaring hawks Buteo jamaicensis and Buteo swainsoni as models, we show that the SPD is not integral for ventilation, that an inflated SPD can increase the moment arm of cranial parts of the pectoralis, and that pectoralis muscle fascicles are significantly shorter in soaring hawks than in non-soaring birds. This coupling of an SPD-mediated increase in pectoralis leverage with force-specialized muscle architecture produces a pneumatic system that is adapted for the isometric contractile conditions expected in soaring flight. The discovery of a mechanical role for the respiratory system in avian locomotion underscores the functional complexity and heterogeneity of this organ system, and suggests that pulmonary diverticula are likely to have other undiscovered secondary functions. These data provide a mechanistic explanation for the repeated appearance of the SPD in soaring lineages and show that the respiratory system can be co-opted to provide biomechanical solutions to the challenges of flight and thereby influence the evolution of avian volancy.

Torsional and axial compressive properties of tibiotarsal bones of red-tailed hawks (Buteo jamaicensis).

OBJECTIVE To describe the torsional and axial compressive properties of tibiotarsal bones of red-tailed hawks (Buteo jamaicensis). SAMPLE 16 cadaveric tibiotarsal bones from 8 red-tailed hawks. PROCEDURES 1 tibiotarsal bone from each bird was randomly assigned to be tested in torsion, and the contralateral bone was tested in axial compression. Intact bones were monotonically loaded in either torsion (n = 8) or axial compression (8) to failure. Mechanical variables were derived from load-deformation curves. Fracture configurations were described. Effects of sex, limb side, and bone dimensions on mechanical properties were assessed with a mixed-model ANOVA. Correlations between equivalent torsional and compressive properties were determined. RESULTS Limb side and bone dimensions were not associated with any mechanical property. During compression tests, mean ultimate cumulative energy and postyield energy for female bones were significantly greater than those for male bones. All 8 bones developed a spiral diaphyseal fracture and a metaphyseal fissure or fracture during torsional tests. During compression tests, all bones developed a crushed metaphysis and a fissure or comminuted fracture of the diaphysis. Positive correlations were apparent between most yield and ultimate torsional and compressive properties. CONCLUSIONS AND CLINICAL RELEVANCE The torsional and axial compressive properties of tibiotarsal bones described in this study can be used as a reference for investigations into fixation methods for tibiotarsal fractures in red-tailed hawks. Although the comminuted and spiral diaphyseal fractures induced in this study were consistent with those observed in clinical practice, the metaphyseal disruption observed was not and warrants further research.

Extraocular muscle architecture in hawks and owls.

OBJECTIVE: A complete and accurate understanding of extraocular muscle function is important to the veterinary care of the avian eye. This is especially true for birds of prey, which rely heavily on vision for survival and yet are prone to ocular injury and disease. To better understand the function of extraocular muscles in birds of prey, we studied extraocular muscle architecture grossly and histologically. ANIMALS STUDIED: This sample was composed of two each of the following species: red-tailed hawk (Buteo jamaicensis), Harris's hawk (Parabuteo unicinctus), great horned owl (Bubo virginianus), and barn owl (Tyto alba). PROCEDURES: All extraocular muscles were dissected and weighed. To analyze muscle fiber architecture, the superior oblique and quadratus muscles were dissected, weighed, and sectioned at 5 µm thickness in the transverse plane. We calculated the physiologic cross-sectional area and the ratio of muscle mass to predicted effective maximum tetanic tension. RESULTS AND CONCLUSIONS: Hawk and owl extraocular muscles exhibit significant physiological differences that play roles in ocular movements and closure of the nictitating membrane. Owls, which do not exhibit extraocular movement, have muscle architecture suited to stabilize the position of a massive, tubular eye that protrudes significantly from the orbit. Hawks, which have a more globose eye that is largely contained within the orbit, do not require as much muscular stability and instead have muscle architecture that facilitates rapid eye movement.

Bioinspired wingtip devices: a pathway to improve aerodynamic performance during low Reynolds number flight.

Birds are highly capable and maneuverable fliers, traits not currently shared with current small unmanned aerial vehicles. They are able to achieve these flight capabilities by adapting the shape of their wings during flight in a variety of complex manners. One feature of bird wings, the primary feathers, separate to form wingtip gaps at the distal end of the wing. This paper presents bio-inspired wingtip devices with varying wingtip gap sizes, defined as the chordwise distance between wingtip devices, for operation in low Reynolds number conditions of Re = 100 000, where many bird species operate. Lift and drag data was measured for planar and nonplanar wingtip devices with the total wingtip gap size ranging from 0% to 40% of the wing's mean chord. For a planar wing with a gap size of 20%, the mean coefficient of lift in the pre-stall region is increased by 7.25%, and the maximum coefficient of lift is increased by 5.6% compared to a configuration with no gaps. The nonplanar wingtip device was shown to reduce the induced drag. The effect of wingtip gap sizes is shown to be independent of the planarity/nonplanarity of the wingtip device, thereby allowing designers to decouple the wingtip parameters to tune the desired lift and drag produced.

Using Hawkeye from the Avengers to communicate on the eye.

Superheroes, such as Iron Man, Captain America, Wonder Woman, Batman, and Hawkeye, have appeared in numerous films, displaying their range of incredible superpowers and abilities. Therefore, it is unsurprising that many people would not only wish to attain these powers, but also to learn about scientific accessibility to these powers. Popular culture characters such as superheroes can provide a unique platform for the communication of difficult scientific concepts. In the classroom, these characters can be used to communicate learning objectives to students in an interesting, fun, and accessible manner by taking advantage of student familiarity with the characters. Hawkeye, a member of the Avengers, is one such superhero who can be utilized by educators. His powers can be attributed in part to his advanced eyesight, which has physiological aspects in common with many birds of prey. Hence, Hawkeye can instigate discussion on the physiology of the human eye, while also allowing for comparison with other species, such as birds of prey, and reflection on advancements related to genetic engineering and wearable technologies. In addition, in my experience, Hawkeye has proven to be a highly suitable popular culture character for use in scientific communication and outreach.

Sexual dimorphism in jaw muscles of the Japanese sparrowhawk (Accipiter gularis).

Materials suitable for anatomical research of raptorial birds are rare. Bird-eating raptors show distinct inter-sexual differences in body size and parental roles. The large females catch larger prey and prepare small morsels to feed their young using their hooked beaks. Here, we investigated the architectural properties of different jaw muscles of the Japanese sparrowhawk (Accipiter gularis) and examined whether there is sexual dimorphism in their architectural design. The results showed that musculus depressor mandibulae, the opener of the lower jaw, was characterized by relatively long fascicle length, whereas musculus pterygoideus was characterized by its larger mass and physiological cross-sectional area (PCSA) in both sexes. Females have the potential capacity to produce rapid and strong bites by their significantly longer fascicle length of M. depressor mandibulae and larger mass and PCSA of M. pterygoideus. For body size-matched gender, jaw muscles of males had fibres of relatively longer length than females, enabling greater velocity and excursion. Architectural characteristics of jaw muscles, together with the absolute dimorphism (the fascicle length of M. depressor mandibulae, the muscle mass and PCSA of M. pterygoideus) and relative dimorphism in the muscle mass of M. pterygoideus, reflect dietary difference and asymmetric parental roles between the sexes.

Macroanatomical Aspects of the Lumbar Plexus and its Branches in the Sparrowhawk.

This study examined the plexus lumbalis and its branches in the sparrowhawk (Accipiter nisus). Fifteen sparrowhawks were used in this study. After administering an anaesthetic to the birds, the body cavities were opened. The birds were fixed with formaldehyde after draining of the blood. The nerves of the plexus lumbalis were dissected separately and photographed. The plexus lumbalis was formed by the union of the branches of the synsacral spinal nerves, which left from the ventrolaterale of os lumbosacrale. The plexus consisted of three (2nd, 3rd and 4th) synsacral spinal nerves. The cranial and caudal nerves originating from the plexus lumbalis were the nervus cutaneous femoris, nervus coxalis cranialis, nervus femoralis, nervus saphenus and nervus obturatorius. The general macroanatomical shape of the plexus lumbalis and the distribution of the nerves originating from this plexus were similar to those of other bird species.

Observations on the right ovary of birds of prey: a histological and immunohistochemical study.

In most avian species, only the left ovary and oviduct are developed in the adult bird. Right ovaries and oviducts usually do not mature further after hatching and remain only rudimentary. However, occurrence of a functional right ovary is frequently found in several species of birds of prey. In this study, we investigated the occurrence of the right ovaries and their morphology in these bird species. Four examined wild bird species possessed a right ovary: long-eared owl, common buzzard, sparrow hawk and goshawk. We used histological and immunohistochemical techniques to evaluate structural differences of the gonads and tried to correlate the findings with folliculogenesis and endocrine functions. The right ovaries showed different sizes and shapes. Cytoskeletal elements (tubulin and vimentin) and α-smooth muscle actin have been detected in different structures of the right ovaries, but their staining intensity was weaker compared with the left ovary. This shows that also the right ovary is mechanically able to ovulate. We could also demonstrate the expression of oestrogen receptor α and progesterone receptor in the right ovaries, which indicates that also the right ovary can respond to steroid hormone stimuli. We assume that the expression of steroid hormone receptors in the presumptive gonad is still sufficient to mediate the development of a right ovary in the studied species. We conclude that the expression of steroid hormone receptors in the right ovary is involved in its post-natal development. The histological and immunohistochemical data also imply that in the right ovary, folliculogenesis and ovulation can occur.

Microstructure and cross-sectional shape of limb bones in Great Horned Owls and Red-tailed Hawks: how do these features relate to differences in flight and hunting behavior?

The Red-tailed Hawk and Great Horned Owl are two species of raptor that are similar in body size, diet, and habitat. Both species use their hindlimbs during hunting, but differ in foot morphology, how they approach and immobilize prey, and the average size of prey captured. They also differ in primary flight style: the Red-tailed Hawk uses static soaring and the Great Horned Owl uses flap-gliding. The objectives of this study were to characterize the microstructure and cross-sectional shape of limb bones of these species and examine the relationship with flight and hunting behaviors. The mid-shaft of six limb bones from six individuals of each species was sampled. The degree of bone laminarity (proportion of circular primary vascular canals) and cross-sectional geometric parameters were calculated. In both species, the humerus and femur exhibited features that suggest high resistance to torsional loading, whereas the tibiotarsus and phalanges had a shape more likely to resist compression and bending in a specific plane. The femur of the Red-tailed Hawk exhibited higher laminarity and larger polar moment of area than that of the Great Horned Owl. The tibiotarsus was more elliptical than that of the Great Horned Owl. The hawk approaches prey from a more horizontal axis, takes prey of greater mass, and is more likely to pursue prey on the ground, which could potentially be causing more torsional loads on the femur and bending loads on the tibiotarsus. In addition, differences in polar moment of area of the phalanges between the species could relate to differences in foot morphology or digit length. The humerus and ulna of the flap-gliding Great Horned Owl are more elliptical than the static soaring Red-tailed Hawk, a shape that may better resist the bending loads associated with a larger amount of flapping.

Comparison of transcoelomic, contrast transcoelomic, and transesophageal echocardiography in anesthetized red-tailed hawks (Buteo jamaicensis).

OBJECTIVE: To assess the agreement and reliability of cardiac measurements obtained with 3 echocardiographic techniques in anesthetized red-tailed hawks (Buteo jamaicensis). ANIMALS: 10 red-tailed hawks. PROCEDURES: Transcoelomic, contrast transcoelomic, and transesophageal echocardiographic evaluations of the hawks were performed, and cineloops of imaging planes were recorded. Three observers performed echocardiographic measurements of cardiac variables 3 times on 3 days. The order in which hawks were assessed and echocardiographic techniques were used was randomized. Results were analyzed with linear mixed modeling, agreement was assessed with intraclass correlation coefficients, and variation was estimated with coefficients of variation. RESULTS: Significant differences were evident among the 3 echocardiographic methods for most measurements, and the agreement among findings was generally low. Interobserver agreement was generally low to medium. Intraobserver agreement was generally medium to high. Overall, better agreement was achieved for the left ventricular measurements and for the transesophageal approach than for other measurements and techniques. CONCLUSIONS AND CLINICAL RELEVANCE: Echocardiographic measurements in hawks were not reliable, except when the left ventricle was measured by the same observer. Furthermore, cardiac morphometric measurements may not be clinically important. When measurements are required, one needs to consider that follow-up measurements should be performed by the same echocardiographer and should show at least a 20% difference from initial measurements to be confident that any difference is genuine.

A comparative study of the mechanics of the pectoralis muscle of the red-tailed hawk and the barred owl.

A comparison of the isometric forces and levers of the pectoralis muscle in red-tailed hawks (Buteo jamaicensis) and barred owls (Strix varia) was done to identify differences that may correlate with their different flight styles. The pectoralis consists of two heads, the anterior m. sternobrachialis (SB) and the posterior m. thoracobrachialis (TB). These are joined at an intramuscular tendon and are supplied by separate primary nerve branches. As in other birds, the two heads have distinct fiber orientations in red-tailed hawks and barred owls. SB's fiber orientation (posterolateral and mediolateral from origin to insertion) provides pronation and protraction of the humerus during adduction. Electromyographic studies in pigeons show that it is active in early downstroke and during level flight. TB is more active during take-off and landing in pigeons. The anterolateral orientation (from origin to insertion) of its fibers provides a retractive component to humeral adduction used to control the wing during landing. In our study, the maximum isometric force produced by the combined pectoralis heads did not differ significantly between the hawk and owl, however, the forces were distributed differently between the two muscle heads. In the owl, SB and TB were capable of producing equal amounts of force, but in the hawk, SB produced significantly less force than did TB. This may reflect the need for a large TB to control landing in both birds during prey-strike, with the owl maintaining both protractive (using SB) and retractive (using TB) abilities. Pronation and protraction may be less important in the flight behavior of the hawk, but its prey-strike behavior may require the maintenance of a substantial TB for braking and controlled stalling, as it initiates strike behavior.

Adaptive significance of permanent female mimicry in a bird of prey.

Permanent female mimicry, in which adult males express a female phenotype, is known only from two bird species. A likely benefit of female mimicry is reduced intrasexual competition, allowing female-like males to access breeding resources while avoiding costly fights with typical territorial males. We tested this hypothesis in a population of marsh harriers Circus aeruginosus in which approximately 40 per cent of sexually mature males exhibit a permanent, i.e. lifelong, female plumage phenotype. Using simulated territorial intrusions, we measured aggressive responses of breeding males towards conspecific decoys of females, female-like males and typical males. We show that aggressive responses varied with both the type of decoys and the type of defending male. Typical males were aggressive towards typical male decoys more than they were towards female-like male decoys; female-like male decoys were attacked at a rate similar to that of female decoys. By contrast, female-like males tolerated male decoys (both typical and female-like) and directed their aggression towards female decoys. Thus, agonistic responses were intrasexual in typical males but intersexual in female-like males, indicating that the latter not only look like females but also behave like them when defending breeding resources. When intrasexual aggression is high, permanent female mimicry is arguably adaptive and could be seen as a permanent 'non-aggression pact' with other males.

Plumage polymorphism and fitness in Swainson's hawks.

We examine the maintenance of a plumage polymorphism, variation in plumages among the same age and sex class within a population, in a population of Swainson's Hawks. We take advantage of 32 years of data to examine two prevalent hypotheses used to explain the persistence of morphs: apostatic selection and heterozygous advantage. We investigate differences in fitness among three morph classes of a melanistic trait in Swainson's Hawks: light (7% of the local breeding population), intermediate (57%) and dark (36%). Specifically, we examined morph differences in adult apparent survival, breeding success, annual number of fledglings produced, probability of offspring recruitment into the breeding population and lifetime reproductive success (LRS). If apostatic selection were a factor in maintaining morphs, we would expect that individuals with the least frequent morph would perform best in one or more of these fitness categories. Alternatively, if heterozygous advantage played a role in the maintenance of this polymorphism, we would expect heterozygotes (i.e. intermediate morphs) to have one or more increased rates in these categories. We found no difference in adult apparent survival between morph classes. Similarly, there were no differences in breeding success, nest productivity, LRS or probability of recruitment of offspring between parental morph. We conclude that neither apostatic selection nor heterozygous advantage appear to play a role in maintaining morphs in this population.

In vivo bite and grip forces, morphology and prey-killing behavior of North American accipiters (Accipitridae) and falcons (Falconidae).

Raptors exhibit a diversity of strategies to procure their prey but ultimately kill using their beaks and/or talons. Thus, bite and grip forces are ecologically important variables that have direct survival implications. Whereas hawks rely primarily on their feet for killing prey, falcons tend to employ their beaks. Consequently, falcons are expected to achieve relatively greater bite forces, and hawks are expected to generate relatively greater grip forces. Force estimates predicted from musculoskeletal morphology in a previous study indicated that falcons (Falco spp.) possess greater jaw force capabilities than accipiters (Accipiter spp.) but there were no clear differences in predicted grip-force capacity outside of differences in scaling. The objective of this study was to complement those results with measurements of in vivo forces by inducing captive and wild accipiters and falcons to bite and grasp force transducers. Bite force increased isometrically in both groups whereas grip force tended toward positive allometry. After adjusting for body mass, falcons produced greater bite forces, and accipiters produced greater grip forces. Thus, previous anatomical estimates of forces predicted the expected direction and magnitude of differences in bite forces but the overall greater in vivo grip forces of accipiters deviated from the pattern obtained from biomechanical estimates. Although the scaling relationships were similar between data sets, forces generated by live birds were consistently lower than those predicted from biomechanics. Estimated and in vivo jaw and digital forces were nevertheless correlated, and therefore provide an important link between morphology and killing behavior in these raptors.

Retinal structure of birds of prey revealed by ultra-high resolution spectral-domain optical coherence tomography.

PURPOSE: To reveal three-dimensional (3-D) information about the retinal structures of birds of prey in vivo. METHODS: An ultra-high resolution spectral-domain optical coherence tomography (SD-OCT) system was built for in vivo imaging of retinas of birds of prey. The calibrated imaging depth and axial resolution of the system were 3.1 mm and 2.8 µm (in tissue), respectively. 3-D segmentation was performed for calculation of the retinal nerve fiber layer (RNFL) map. RESULTS: High-resolution OCT images were obtained of the retinas of four species of birds of prey: two diurnal hawks (Buteo platypterus and Buteo brachyurus) and two nocturnal owls (Bubo virginianus and Strix varia). These images showed the detailed retinal anatomy, including the retinal layers and the structure of the deep and shallow foveae. The calculated thickness map showed the RNFL distribution. Traumatic injury to one bird's retina was also successfully imaged. CONCLUSIONS: Ultra-high resolution SD-OCT provides unprecedented high-quality 2-D and 3-D in vivo visualization of the retinal structures of birds of prey. SD-OCT is a powerful imaging tool for vision research in birds of prey.

A low false negative filter for detecting rare bird species from short video segments using a probable observation data set-based EKF method.

We report a new filter to assist the search for rare bird species. Since a rare bird only appears in front of a camera with very low occurrence (e.g., less than ten times per year) for very short duration (e.g., less than a fraction of a second), our algorithm must have a very low false negative rate. We verify the bird body axis information with the known bird flying dynamics from the short video segment. Since a regular extended Kalman filter (EKF) cannot converge due to high measurement error and limited data, we develop a novel probable observation data set (PODS)-based EKF method. The new PODS-EKF searches the measurement error range for all probable observation data that ensures the convergence of the corresponding EKF in short time frame. The algorithm has been extensively tested using both simulated inputs and real video data of four representative bird species. In the physical experiments, our algorithm has been tested on rock pigeons and red-tailed hawks with 119 motion sequences. The area under the ROC curve is 95.0%. During the one-year search of ivory-billed woodpeckers, the system reduces the raw video data of 29.41 TB to only 146.7 MB (reduction rate 99.9995%).

Molecular and morphological divergence in a pair of bird species and their ectoparasites.

In an evolutionary context, parasites tend to be morphologically conservative relative to their hosts. However, the rate of neutral molecular evolution across many parasite lineages is faster than in their hosts. Although this relationship is apparent at the macroevolutionary scale, insight into the processes underpinning it may be gained through investigations at the microevolutionary scale. Birds and their ectoparasitic lice have served as important natural experiments in co-evolution. Here, we compared mitochondrial and morphological divergence in 2 recently diverged avian host lineages and their parasites. Gálapagos hawks (Buteo galapagoensis) are phenotypically divergent from their closest mainland relatives, the Swainson's hawk (Buteo swainsoni). Both species are host to a feather louse species of Craspedorrhynchus (Insecta: Phthiraptera: Ischnocera, Philopteridae). We sequenced the 5' end of the mitochondrial gene cytochrome oxidase c subunit I (COI) from a set of hawks and lice. Although this fragment allowed unambiguous identification of host and parasite lineages on the islands and the mainland, only a single variable site was present in the 2 hosts, but 2 major Craspedorrhynchus clades divergent by ~10% were recovered that sorted perfectly with host species. We found significant population genetic structure within the Galápagos Craspedorrhynchus lineage. While the host species are highly differentiated phenotypically, the 2 Craspedorrhynchus louse lineages are phenotypically overlapping, although subtle but significant morphological differences exist.

Use of random amplified polymorphic DNA to identify several novel markers for sex identification in the crested serpent eagle and crested goshawk.

The crested serpent eagle (Spilornis cheela hoya) has no distinct sexual dimorphic traits. In the current study, we report the results of an EE0.6 (EcoRI 0.6-kb fragment) sequence applied to S. cheela hoya and a novel random amplified polymorphic DNA (RAPD) marker that can be used to sex individuals within the species S. cheela hoya and Accipiter trivigatus formosae (crested goshawk). We used sex-specific primers for the avian CHD1 (chromo-helicase-DNA-binding 1) gene and the EE0.6 sequence in PCR assays to determine sex. In addition, 120 random primers were used for RAPD fingerprinting to search for novel sex-specific fragments of S. cheela hoya. The OPBB08 random primer generated a 1241-bp sex-specific fragment in all female S. cheela hoya. From the nucleotide sequence, PCR primers were designed to amplify 553-, 895-, and 194-bp sex-specific fragments present in all female S. cheela hoya. One of these primer pairs (ScBB08-7F/R) also amplified a male/female common fragment that can be used as an internal control (543bp). Moreover, one of the primer pairs (ScBB08-5aF/5bR) could be used to identify genders of A. trivigatus formosae. In conclusion, we identified novel sex-specific DNA markers of S. cheela hoya and A. trivigatus formosae that can be used for rapid and accurate sex identification.

[SEM studies on the connective tissue cores of the lingual papillae of the northern goshawk (Accipiter gentilis)].

The lingual papillae and their connective tissue cores (CTCs) of the northern goshawk were examined by scanning electron microscopy (SEM). The length of the tongue was approximately 2.5 cm. The median groove divided the body of the tongue into symmetrical parts. At a point approximately 2/3 of the length, there were large conical papillae between the body and the root of the tongue, the apices of which were pointed towards the posterior part of the tongue. Under the light microscopy, the filiform papillae of the dorsal surface in the lingual body showed the desquamate cells of non-keratinized epithelium. There were openings of the lingual glands on the anterior part and root of the tongue. The lingual papillae and their CTCs of the northern goshawk had a structure similar to those of the white tailed eagle and black kite.

Nutritional condition and serum biochemistry for free-living Swainson's Hawks wintering in central Argentina.

We assessed the nutritional condition and established reference values for serum chemistry parameters in a long distance migrant bird of prey, the Swainson's Hawk (Buteo swainsoni), wintering in central Argentina. We analyzed serum concentration of urea, uric acid, cholesterol, and triglycerides and assessed age and sex related differences in these parameters. A body condition index was obtained from the resultant residuals of the regression of body mass and a morphometric measure. No statistical differences were observed among sex and age groups for urea, uric acid and triglyceride serum concentration. However, cholesterol concentration differed among male and female hawks, which could be related to the gain of body mass in wintering grounds at differential rates. The mean values of the four parameters were in the range of those recorded in the Common Buzzard (Buteo buteo), indicating good nutritional condition of the population we studied. Forearm length was the morphometric variable that better correlated with body mass. The resultant body condition index was only correlated with triglyceride concentration, suggesting that this index could be valuable in future work dealing with the assessment of body fat storage in wintering and breeding hawks, as well as in stopover points on the migratory route.