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.

Optimization of avian perching manoeuvres.

Perching at speed is among the most demanding flight behaviours that birds perform1,2 and is beyond the capability of most autonomous vehicles. Smaller birds may touch down by hovering3-8, but larger birds typically swoop up to perch1,2-presumably because the adverse scaling of their power margin prohibits hovering9 and because swooping upwards transfers kinetic to potential energy before collision1,2,10. Perching demands precise control of velocity and pose11-14, particularly in larger birds for which scale effects make collisions especially hazardous6,15. However, whereas cruising behaviours such as migration and commuting typically minimize the cost of transport or time of flight16, the optimization of such unsteady flight manoeuvres remains largely unexplored7,17. Here we show that the swooping trajectories of perching Harris' hawks (Parabuteo unicinctus) minimize neither time nor energy alone, but rather minimize the distance flown after stalling. By combining motion capture data from 1,576 flights with flight dynamics modelling, we find that the birds' choice of where to transition from powered dive to unpowered climb minimizes the distance over which high lift coefficients are required. Time and energy are therefore invested to provide the control authority needed to glide safely to the perch, rather than being minimized directly as in technical implementations of autonomous perching under nonlinear feedback control12 and deep reinforcement learning18,19. Naive birds learn this behaviour on the fly, so our findings suggest a heuristic principle that could guide reinforcement learning of autonomous perching.

High aerodynamic lift from the tail reduces drag in gliding raptors.

Many functions have been postulated for the aerodynamic role of the avian tail during steady-state flight. By analogy with conventional aircraft, the tail might provide passive pitch stability if it produced very low or negative lift. Alternatively, aeronautical principles might suggest strategies that allow the tail to reduce inviscid, induced drag: if the wings and tail act in different horizontal planes, they might benefit from biplane-like aerodynamics; if they act in the same plane, lift from the tail might compensate for lift lost over the fuselage (body), reducing induced drag with a more even downwash profile. However, textbook aeronautical principles should be applied with caution because birds have highly capable sensing and active control, presumably reducing the demand for passive aerodynamic stability, and, because of their small size and low flight speeds, operate at Reynolds numbers two orders of magnitude below those of light aircraft. Here, by tracking up to 20,000, 0.3 mm neutrally buoyant soap bubbles behind a gliding barn owl, tawny owl and goshawk, we found that downwash velocity due to the body/tail consistently exceeds that due to the wings. The downwash measured behind the centreline is quantitatively consistent with an alternative hypothesis: that of constant lift production per planform area, a requirement for minimizing viscous, profile drag. Gliding raptors use lift distributions that compromise both inviscid induced drag minimization and static pitch stability, instead adopting a strategy that reduces the viscous drag, which is of proportionately greater importance to lower Reynolds number fliers.

Seasonal Dynamics of Testosterone and Corticosterone in Predatory Birds as Exemplified by the Northern Goshawk (Accipiter gentilis).

Testosterone and corticosterone are steroid hormones that regulate various aspects of bird behavior. The dynamics of blood level of these hormones depending on the stage of the life cycle have been studied in many species. It has been shown for both sexes that the levels of both hormones rise during the breeding season. We have studied changes in the level of these hormones in the northern goshawk (Accipiter gentilis) during a year. This has been the first study of this type on northern goshawk. We collected blood samples from 16 adult northern goshawks kept in pairs in aviaries in the VITASFERA Rare Bird Species Breeding Center. The testosterone level rises in males during the period of lekking and mating (March-June); however, there is no synchronous increase in females. The corticosterone level generally remains high throughout the year in both sexes. Since these are the only data on the northern goshawk, it cannot be concluded whether this is characteristic of the species as a whole or only for captive birds.

Auditory performance in bald eagles and red-tailed hawks: a comparative study of hearing in diurnal raptors.

Collision with wind turbines is a conservation concern for eagles with population abundance implications. The development of acoustic alerting technologies to deter eagles from entering hazardous air spaces is a potentially significant mitigation strategy to diminish associated morbidity and mortality risks. As a prelude to the engineering of deterrence technologies, auditory function was assessed in bald eagles (Haliaeetus leucocephalus), as well as in red-tailed hawks (Buteo jamaicensis). Auditory brainstem responses (ABRs) to a comprehensive battery of clicks and tone bursts varying in level and frequency were acquired to evaluate response thresholds, as well as suprathreshold response characteristics of wave I of the ABR, which represents the compound potential of the VIII cranial nerve. Sensitivity curves exhibited an asymmetric convex shape similar to those of other avian species, response latencies decreased exponentially with increasing stimulus level and response amplitudes grew with level in an orderly manner. Both species were responsive to a frequency band at least four octaves wide, with a most sensitive frequency of 2 kHz, and a high-frequency limit of approximately 5.7 kHz in bald eagles and 8 kHz in red-tailed hawks. Findings reported here provide a framework within which acoustic alerting signals might be developed.

Prey abundance and urbanization influence the establishment of avian predators in a metropolitan landscape.

Urbanization causes the simplification of natural habitats, resulting in animal communities dominated by exotic species with few top predators. In recent years, however, many predators such as hawks, and in the US coyotes and cougars, have become increasingly common in urban environments. Hawks in the Accipiter genus, especially, are recovering from widespread population declines and are increasingly common in urbanizing landscapes. Our goal was to identify factors that determine the occupancy, colonization and persistence of Accipiter hawks in a major metropolitan area. Through a novel combination of citizen science and advanced remote sensing, we quantified how urban features facilitate the dynamics and long-term establishment of Accipiter hawks. Based on data from Project FeederWatch, we quantified 21 years (1996-2016) of changes in the spatio-temporal dynamics of Accipiter hawks in Chicago, IL, USA. Using a multi-season occupancy model, we estimated Cooper's (Accipiter cooperii) and sharp-shinned (A. striatus) hawk occupancy dynamics as a function of tree canopy cover, impervious surface cover and prey availability. In the late 1990s, hawks occupied 26% of sites around Chicago, but after two decades, their occupancy fluctuated close to 67% of sites and they colonized increasingly urbanized areas. Once established, hawks persisted in areas with high levels of impervious surfaces as long as those areas supported high abundances of prey birds. Urban areas represent increasingly habitable environments for recovering predators, and understanding the precise urban features that drive colonization and persistence is important for wildlife conservation in an urbanizing world.

Visual field shape and foraging ecology in diurnal raptors.

Birds, particularly raptors, are believed to forage primarily using visual cues. However, raptor foraging tactics are highly diverse - from chasing mobile prey to scavenging - which may reflect adaptations of their visual systems. To investigate this, we studied the visual field configuration of 15 species of diurnal Accipitriformes that differ in such tactics, first focusing on the binocular field and blind area by using a single-traits approach, and then exploring the shape of the binocular field with a morphometric approach. While the maximum binocular field width did not differ between species with different foraging tactics, the overall shape of their binocular fields did. In particular, raptors chasing terrestrial prey (ground predators) had a more protruding binocular field and a wider blind area above the head than did raptors chasing aerial or aquatic prey and obligate scavengers. Ground predators that forage on mammals from above have a wide but short bill - which increases ingestion rate - and a large suborbital ridge to avoid sun glare. This may explain the protruding binocular field and the wide blind area above the head. By contrast, species from the two other groups have long but narrow bills used to pluck, flake or tear food and may need large visual coverage (and reduced suborbital ridges) to increase their foraging efficiency (e.g. using large visual coverage to follow the escaping prey in three dimensions or detect conspecifics). We propose that binocular field shape is associated with bill and suborbital ridge shape and, ultimately, foraging strategies.

Discovering the effect of nonlocal payoff calculation on the stabilty of ESS: Spatial patterns of Hawk-Dove game in metapopulations.

The classical idea of evolutionarily stable strategy (ESS) modeling animal behavior does not involve any spatial dependence. We considered a spatial Hawk-Dove game played by animals in a patchy environment with wrap around boundaries. We posit that each site contains the same number of individuals. An evolution equation for analyzing the stability of the ESS is found as the mean dynamics of the classical frequency dependent Moran process coupled via migration and nonlocal payoff calculation in 1D and 2D habitats. The linear stability analysis of the model is performed and conditions to observe spatial patterns are investigated. For the nearest neighbor interactions (including von Neumann and Moore neighborhoods in 2D) we concluded that it is possible to destabilize the ESS of the game and observe pattern formation when the dispersal rate is small enough. We numerically investigate the spatial patterns arising from the replicator equations coupled via nearest neighbor payoff calculation and dispersal.

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.

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.

Seasonal detours by soaring migrants shaped by wind regimes along the East Atlantic Flyway.

Avian migrants often make substantial detours between their seasonal destinations. It is likely some species do this to make the most of predictable wind regimes along their respective flyways. We test this hypothesis by studying orientation behaviour of a long-distance soaring migrant in relation to prevailing winds along the East Atlantic Flyway. We tracked 62 migratory journeys of 12 adult European Honey Buzzards Pernis apivorus with GPS loggers. Hourly fixes were annotated with local wind vectors from a global atmospheric model to determine orientation behaviours with respect to the buzzards' seasonal goal destinations. This enabled us to determine hot spots where buzzards overdrifted and overcompensated for side winds. We then determined whether winds along the buzzards' detours differed from winds prevailing elsewhere in the flyway. Honey Buzzards cross western Africa using different routes in autumn and spring. In autumn, they overcompensated for westward winds to circumvent the Atlas Mountains on the eastern side and then overdrifted with south-westward winds while crossing the Sahara. In spring, however, they frequently overcompensated for eastward winds to initiate a westward detour at the start of their journey. They later overdrifted with side winds north-westward over the Sahel and north-eastward over the Sahara, avoiding adverse winds over the central Sahara. We conclude that Honey Buzzards make seasonal detours to utilize more supportive winds further en route and thereby expend less energy while crossing the desert. Lifelong tracking studies will be helpful to elucidate how honey buzzards and other migrants learn complex routes to exploit atmospheric circulation patterns from local to synoptic scales.

An assessment of exposure and effects of persistent organic pollutants in an urban Cooper's hawk (Accipiter cooperii) population.

Among the stressors confronting urban wildlife, chemical contaminants pose a particular problem for high trophic feeding species. Previous data from fortuitous carcass collections revealed surprisingly high levels of persistent organic pollutants in raptor species, including the Cooper's hawk (Accipiter cooperii), from urbanized areas of southwestern British Columbia, Canada. Thus, in 2012 and 2013, we followed up on that finding by measuring POPs in blood samples from 21 adult and 15 nestling Cooper's hawks in Vancouver, a large urban area in southwestern Canada. Reproductive success and circulating thyroid hormones were measured to assess possible toxicological effects. Model comparisons showed concentrations of polychlorinated biphenyls (ΣPCBs) were positively influenced by the level of urbanization. Total thyroxin (TT4) was negatively associated with increases in ΣPCBs. Total triiodothyronine (TT3) was negatively associated with ΣPCBs and polybrominated diphenyl ethers (ΣPBDEs). The legacy insecticide, dieldrin, appeared to have some negative influence on reproductive success. There is some evidence of biochemical perturbation by PBDEs and lingering impact of legacy POPs which have not been used for at least 40 years, but overall Cooper's hawks have successfully populated this urban environment.

Changes in the membrane carbohydrates from sperm cryopreserved with dimethylsulfoxide or polyvinylpyrrolidone of red-tailed hawk (Buteo jamaicencis).

BACKGROUND: That cryopreservation can induce alterations in sperm. OBJECTIVE: The goal of this study was to evaluate sperm quality and distribution of N-acetylglucosamine, sialic acid and mannose residues in sperm cryopreserved of red-tailed hawk (Buteo jamaicensis). MATERIALS AND METHODS: We studied twenty samples of ejaculated semen for each cryoprotectant dimethylsulfoxide or polyvinylpyrrolidone. Carbohydrate identification was carried out with lectins Triticum vulgaris agglutinin to N-acetylglucosamine and sialic acid and Concanavalia ensiformis for mannose residues. Sperm viability was not altered but motility decreased significantly with both crioprotectants compared with fresh sperm. RESULTS: Neither the number of WGA positive sperm nor the distribution of N-acetylglucosamine and/or sialic acid residues were affected by the cryopreservation procedure. The sperm proportion with fluorescence associated with the presence of mannose residues was higher in thawed sperm. CONCLUSION: Values obtained with the cryopreservation technique proposed in this study by freezing drops in liquid nitrogen, were within normal parameters established for good quality fresh semen. We can say that it can be used for assisted reproduction of Buteo jamaicensis.

Is multiple nest building an adequate strategy to cope with inter-species nest usurpation?

BACKGROUND: Black sparrowhawks (Accipiter melanoleucus) recently colonised the Cape Peninsula, South Africa, where the species faces competition for their nest sites from Egyptian geese (Alopochen aegyptiaca) which frequently usurp black sparrowhawk nests. In this paper, we test the hypothesis that multiple nest building by black sparrowhawks is a strategy to cope with this competitor, based on a 14-year long term data set. RESULTS: Two main results support the hypothesis: first, the numbers of intact nests per breeding season in black sparrowhawk territories increased as levels of geese interactions increased, specifically when usurpation occurred. Usurpation occurred significantly more often at nests later in the season, and may provide a further explanation for the advancement of the black sparrowhawk breeding season towards earlier breeding attempts which results in an overall extension of the breeding period (over 9 months) that has been found in our study population. Second, nest usurpation had a negative impact on black sparrowhawks' reproductive performance at the 'nest' level, but not at the 'territory' level when multiple nests were available within the same breeding season, suggesting that this strategy was effective for dealing with this competitor. However, our results do not rule out long term negative consequences of these interactions, for example, reduced adult survival rates or reduced lifetime reproductive success, due to the higher energy demand required to build several nests each breeding season. CONCLUSIONS: Our results suggest that black sparrowhawks avoid direct conflict with this large and aggressive competitor and instead choose the passive strategy in allocating more resources to multiple nest building. Our research further highlights the importance of behavioural plasticity, which might be especially important for city-dwelling species in the face of global urbanisation.

Predator encounters have spatially extensive impacts on parental behaviour in a breeding bird community.

Predation risk has negative indirect effects on prey fitness, partly mediated through changes in behaviour. Evidence that individuals gather social information from other members of the population suggests that events in a community may impact the behaviour of distant individuals. However, spatially wide-ranging impacts on individual behaviour caused by a predator encounter elsewhere in a community have not been documented before. We investigated the effect of a predator encounter (hawk model presented at a focal nest) on the parental behaviour of pied flycatchers (Ficedula hypoleuca), both at the focal nest and at nearby nests different distances from the predator encounter. We show that nest visitation of both focal pairs and nearby pairs were affected, up to 3 h and 1 h, respectively. Parents also appeared to compensate initial disrupted feeding by later increasing nest visitation rates. This is the first evidence showing that the behaviour of nearby pairs was affected away from an immediate source of risk. Our results indicate that the impacts of short-term predator encounters may immediately extend spatially to the broader community, affecting the behaviour of distant individuals. Information about predators is probably quickly spread by cues such as intra- and heterospecific alarm calls, in communities of different taxa.

Family morph matters: factors determining survival and recruitment in a long-lived polymorphic raptor.

From an evolutionary perspective, recruitment into the breeding population represents one of the most important life-history stages and ultimately determines the effective population size. In order to contribute to the next generation, offspring must survive to sexual maturity, secure a territory and find a mate. In this study, we explore factors influencing both offspring survival and their subsequent recruitment into the local breeding population in a long-lived urban raptor, the black sparrowhawk (Accipiter melanoleucus). Adult black sparrowhawks show discrete colour polymorphism (dark and light morphs), and in South Africa, morphs are distributed clinally with the highest proportion of dark morphs (c.75%) present in our study population on the Cape Peninsula. Parental morph was associated with both survival and recruitment. For survival, parental morph combination was important - with young produced by pairs of contrasting morphs having higher survival rates than young fledged from like-pairs. The association between recruitment and morph was more complex; with an interaction between male morph and breeding time, whereby recruitment of offspring from dark morph fathers was more likely when fledging earlier in the season. The opposite relationship was found for light morph fathers, with their offspring more likely to be recruited if fledged later in the season. This interaction may be due to differential morph-specific hunting success of fathers (males contribute most food provisioning), linked to background matching and crypsis in different weather conditions. Dark morph males may hunt more successfully in rainier and cloudier conditions, which occur more frequently earlier in the breeding season, and light morph males may be more successful later on, when weather conditions become increasingly brighter and drier. Our results reveal a complex situation whereby the family morph combination influences survival, and the father morphs specifically recruitment, revealing morph-specific benefits dependent on the timing of breeding. These empirical data are among the first to support the idea that differential fitness consequence of morph combination may explain balanced polymorphism in a vertebrate population.

Intraguild predation and competition impacts on a subordinate predator.

Intraguild (IG) predation and interspecific competition may affect the settlement and success of species in their habitats. Using data on forest-dwelling hawks from Finland, we addressed the impact of an IG predator, the northern goshawk Accipiter gentilis (goshawk), on the breeding of an IG prey, the common buzzard Buteo buteo. We hypothesized that the subordinate common buzzard avoids breeding in the proximity of goshawks and that interspecific competitors, mainly Strix owls, may also disturb common buzzards by competing for nests and food. Our results show that common buzzards more frequently occupied territories with a low IG predation threat and with no interspecific competitors. We also observed that common buzzards avoided territories with high levels of grouse, the main food of goshawks, possibly due to a risk of IG predation since abundant grouse can attract goshawks. High levels of small rodents attracted interspecific competitors to common buzzard territories and created a situation where there was not only an abundance of food but also an abundance of competitors for the food. These results suggest interplay between top-down and bottom-up processes which influence the interactions between avian predator species. We conclude that the common buzzard needs to balance the risks of IG predation and interference competition with the availability of its own resources. The presence of other predators associated with high food levels may impede a subordinate predator taking full advantage of the available food. Based on our results, it appears that interspecific interactions with dominant predators have the potential to influence the distribution pattern of subordinate predators.

Changes in Physiologic Parameters and Effects of Hooding in Red-tailed Hawks ( Buteo jamaicensis ) During Manual Restraint.

Manual restraint in birds of prey is required for many veterinary and research procedures. To investigate the effects of handling stress on physiologic parameters in raptorial birds, 8 red-tailed hawks ( Buteo jamaicensis ) were manually restrained over a 15-minute period. Respiratory rate (RR), heart rate (HR), and cloacal temperature were monitored over time and recorded at defined intervals during the experiment. The effect of hooding on physiologic variables was also evaluated in a complete crossover design. Both RR and HR decreased significantly during the 15-minute restraint period (HR, -80 ± 101.4 beats/min [bpm], [P < .01]; RR, -17.5 ± 22.6 breaths/min, [P < .05]). Hooded birds had significantly lower HRs and RRs at 15 minutes of restraint (HR: 232.5 ± 26 bpm, [P < .037]; RR: 33.1 ± 6.7 breaths/min, [P < .05]) compared to birds restrained without a hood (HR: 280 ± 74.1 bpm; RR: 51.5 ± 28.8 breaths/min). Cloacal temperature increased significantly in all manually restrained birds (+2.2 ± 0.7°C, [P < .01]), with a comparable increase in hooded and nonhooded birds. In this study of the effects of manual restraint on red-tailed hawks, hooding versus nonhooding amplified the decrease in HR and RR but had no effect on stress-induced hyperthermia.

Parental risk management in relation to offspring defence: bad news for kids.

Do parents defend their offspring whenever necessary, and do self-sacrificing parents really exist? Studies recognized that parent defence is dynamic, mainly depending on the threat predators pose. In this context, parental risk management should consider the threat to themselves and to their offspring. Consequently, the observed defence should be a composite of both risk components. Surprisingly, no study so far has determined the influence of these two threat components on parental decision rules. In a field experiment, we investigated parental risk taking in relation to the threat posed to themselves and their offspring. To disentangle the two threat components, we examined defence behaviours of parent blue tits Cyanistes caeruleus towards three different predators and during different nestling developmental stages. Nest defence strategies in terms of alarm call intensity and nearest predator approach differed between the three predators. Defence intensity was only partly explained by threat level. Most importantly, parental risk management varied in relation to their own, but not offspring risk. Parent defence investment was independent of nestling risk when parents followed a high-risk strategy. However, parents considered nestling as well as parental risk when following a low-risk strategy. Our findings could have general implications for the economy of risk management and decision-making strategies in living beings, including humans.