Correlated evolution of beak and braincase morphology is present only in select bird clades.

Complex morphological structures, such as skulls or limbs, are often composed of multiple morphological components (e.g., bones, sets of bones) that may evolve in a covaried manner with one another. Previous research has reached differing conclusions on the number of semi-independent units, or modules, that exist in the evolution of structures and on the strength of the covariation, or integration, between these hypothesized modules. We focus on the avian skull as an example of a complex morphological structure for which highly variable conclusions have been reached in the numerous studies analyzing support for a range of simple to complex modularity hypotheses. We hypothesized that past discrepancies may stem from both the differing densities of data used to analyze support for modularity hypotheses and the differing taxonomic levels of study. To test these hypotheses, we applied a comparative method to 3D geometric morphometric data collected from the skulls of a diverse order of birds (the Charadriiformes) to test support for 11 distinct hypotheses of modular skull evolution. Across all Charadriiformes, our analyses suggested that charadriiform skull evolution has been characterized by the semi-independent, but still correlated, evolution of the beak from the rest of the skull. When we adjusted the density of our morphometric data, this result held, but the strength of the signal varied substantially. Additionally, when we analyzed subgroups within the order in isolation, we found support for distinct hypotheses between subgroups. Taken together, these results suggest that differences in the methodology of past work (i.e., statistical method and data density) as well as clade-specific dynamics may be the reasons past studies have reached varying conclusions.

Joint extension speed dictates bio-inspired morphing trajectories for optimal longitudinal flight dynamics.

Avian wing morphing allows dynamic, active control of complex flight manoeuvres. Previous linear time-invariant (LTI) models have quantified the effect of varying fixed wing configurations but the time-dependent effects of morphing between different configurations is not well understood. To fill this gap, I implemented a linear parameter-varying (LPV) model for morphing wing gull flight. This approach models the wing joint angles as scheduled parameters and accounts for nonlinear kinematic and gravitational effects while interpolating between LTI models at discrete trim points. With the resulting model, I investigated the longitudinal response associated with various joint extension trajectories. By optimizing the extension trajectory for four independent objectives (speed and pitch angle overshoot, speed rise time and pitch angle settling time), I found that the extension trajectory inherent to the gull wing does not guarantee an optimal response but may provide a sufficient response with a simpler mechanical implementation. Furthermore, the results indicated that gulls likely require extension speed feedback. This morphing LPV model provides insights into underlying control mechanisms, which may allow for avian-like flight in future highly manoeuvrable uncrewed aerial vehicles.

Structure and mechanics of water-holding feathers of Namaqua sandgrouse (Pterocles namaqua).

Desert sandgrouse, such as the Namaqua sandgrouse, nest up to 30 km away from watering holes. Adult male desert sandgrouse have specially adapted feathers on their bellies that hold water, even during flight, allowing the birds to transport water back to the chicks at the nest. The structure of the belly feathers and aspects of the mechanism by which they hold water was first described by Cade and Maclean (Cade, Maclean 1967 Condor 69, 323-343 (doi:10.2307/1366197)). Here, we use scanning electron microscopy and micro-computed tomography as well as videography to characterize the geometry of different components of the belly feathers and to show how differences in their bending stiffnesses contribute to the water-holding mechanism. The results of this study will be used in a companion paper to model computationally water uptake by the feather.

Size variation in mid-Holocene North Atlantic Puffins indicates a dynamic response to climate change.

Seabirds are one of the most at-risk groups, with many species in decline. In Scandinavia, seabirds are at a heightened risk of extinction due to accelerated global warming. Norway is home to significant portion of the European Atlantic Puffin (Fratercula arctica) populations, but Norwegian populations have declined significantly during the last decades. In this paper we use biometric data from modern and archaeological F. arctica specimens to investigate patterns in body size variation over time of this iconic species. We aimed to set out a baseline for our archaeological comparison by firstly investigating whether modern subspecies of F. arctica are reflected in the osteological characters and are enough to distinguish subspecies from the bones alone. We then investigated if archaeological remains of F. arctica differ in size from the modern subspecies. Our results show that the subspecies Fratercula arctica naumanni was distinctly larger than the other subspecies. However, Fratercula arctica arctica and Fratercula arctica grabae were difficult to separate based on size. This generally supports ornithological observations. Post-Medieval F. arctica bones from Måsøy were similar to modern F. a. arctica populations. The mid-Holocene remains from Dollsteinhola overlaps with the modern size ranges of F. a. arctica and F. a. grabae but are generally shorter and more robust. Dollsteinhola is located close to the borders of the modern breeding ranges of both F. a. arctica and F. a. grabae. We consider it therefore likely that given the mid-Holocene climatic oscillations, breeding ranges of the two subspecies shifted north or south accordingly. However, this does not explain the different proportions of the Dollsteinhola specimens. Our data provide the first evidence for shifting distributions in ancient Atlantic Puffins and represent the first osteological analysis of Fratercula arctica subspecies.

Association of insularity and body condition to cloacal bacteria prevalence in a small shorebird.

Do islands harbour less diverse disease communities than mainland? The island biogeography theory predicts more diverse communities on mainland than on islands due to more niches, more diverse habitats and availability of greater range of hosts. We compared bacteria prevalences of Campylobacter, Chlamydia and Salmonella in cloacal samples of a small shorebird, the Kentish plover (Charadrius alexandrinus) between two island populations of Macaronesia and two mainland locations in the Iberian Peninsula. Bacteria were found in all populations but, contrary to the expectations, prevalences did not differ between islands and mainland. Females had higher prevalences than males for Salmonella and when three bacteria genera were pooled together. Bacteria infection was unrelated to bird's body condition but females from mainland were heavier than males and birds from mainland were heavier than those from islands. Abiotic variables consistent throughout breeding sites, like high salinity that is known to inhibit bacteria growth, could explain the lack of differences in the bacteria prevalence between areas. We argue about the possible drivers and implications of sex differences in bacteria prevalence in Kentish plovers.

A comparative ultrastructural study of the pecten oculi in adult, juvenile, and nestling yellow-legged gulls, Larus michahellis (Naumann, 1840).

This study aimed at examining the histological structure of the pecten oculi in the adult yellow-legged gull, Larus michahellis, and at two moments of postnatal development: during the posthatch (nestling) and juvenile periods. Particular attention was paid to differences in the diameter of vessels, the thickness of the basement membrane, and ultrastructural features of endothelial and pigmented stromal cells. Capillary endothelial cells displayed numerous microvillous-like folds projecting from their internal and external surfaces. Intercellular spaces between capillaries were occupied by pigmented stromal cells. The ultrastructure of pecten oculi underwent noticeable changes during postnatal development. The examination of the capillaries in nestlings, juveniles, and adults revealed that the formation process of vessels and pigmented stromal cells did not complete itself in the posthaching phase. The prominent feature of endothelial cells of capillaries in nestlings was that the microvilli were longer than in juvenile and adult cells, and the capillary lumen was therefore reduced. In this sense, their pigmented stromal cells showed fewer melanosomes, lacked intercellular spaces, and cellular junctions could still be observed. These results provide evidence that the pecten oculi during the posthatching phase maintains immature morphological features consistent with a role of pigmented stromal cells in the blood-retina barrier.

Huffin' and puffin: seabirds use large bills to dissipate heat from energetically demanding flight.

Endothermic animals regulate body temperature by balancing metabolic heat production and heat exchange with the environment. Heat dissipation is especially important during and immediately after demanding activities such as flapping flight, the most energetically expensive mode of locomotion. As uninsulated appendages, bird bills present a potential avenue for efficient heat dissipation. Puffins possess large bills and are members of the bird family with the highest known flight cost. Here, we used infrared thermography to test whether wild tufted puffins (Fratercula cirrhata) use their bills to dissipate excess heat after energetically expensive flight. Both bill surface temperature and the proportion of total heat exchange occurring at the bill decreased with time since landing, suggesting that bills are used to dissipate excess metabolic heat. We propose that bill size in puffins may be shaped by opposing selective pressures that include dissipating heat after flight and conserving heat in cold air and water temperatures.

Within-Individual Canalization Contributes to Age-Related Increases in Trait Repeatability: A Longitudinal Experiment in Red Knots.

Age-related increases in the repeatable expression of labile phenotypic traits are often assumed to arise from an increase in among-individual variance due to differences in developmental plasticity or by means of state-behavior feedbacks. However, age-related increases in repeatability could also arise from a decrease in within-individual variance as a result of stabilizing trait expression, that is, canalization. Here we describe age-related changes in within-individual and among-individual variance components in two correlated traits-gizzard mass and exploration behavior-in a medium-sized shorebird, the red knot (Calidris canutus). Increased repeatability of gizzard mass came about due to an increase in among-individual variance, unrelated to differences in developmental plasticity, together with decreases in within-individual variance consistent with canalization. We also found canalization of exploration but no age-related increase in overall repeatability, which suggests that showing predictable expression of exploration behavior may be advantageous from a very young age onward. Contrasts between juveniles and adults in the first year after their capture provide support for the idea that environmental conditions play a key role in generating among-individual variation in both gizzard mass and exploration behavior. Our study shows that stabilization of traits occurs under constant conditions: with increased exposure to predictable cues, individuals may become more certain in their assessment of the environment allowing traits to become canalized.

Consistent declines in wing lengths of Calidridine sandpipers suggest a rapid morphometric response to environmental change.

A recent study demonstrated that semipalmated sandpiper (Calidris pusilla) wing lengths have shortened from the 1980s to the present-day. We examined alternative and untested hypotheses for this change at an important stopover site, James Bay, Ontario, Canada. We evaluated morphometric patterns in wing length and bill length by age and sex, when possible, and assessed if wing shape has also changed during this time-period. We investigated patterns of morphological change in two additional Calidridine sandpipers, white-rumped sandpipers (Calidris fuscicollis) and least sandpipers (Calidris minutilla), to determine if shorter wing lengths are a widespread pattern in small sandpipers. We also examined allometric changes in wing and bill lengths to clarify if wing length declines were consistent with historical scaling relationships and indicative of a change in body size instead of only wing length change. We found that including sex and wing shape in analyses revealed important patterns in morphometric change for semipalmated sandpipers. Wing lengths declined for both sexes, but the magnitude of decline was smaller and not significant for males. Additionally, semipalmated sandpiper wings have become more convex, a shape that increases maneuverability in flight. Wing lengths, but not bill lengths, declined for most species and age classes, a pattern that was inconsistent with historical allometric scaling relationships. For juvenile semipalmated sandpipers, however, both bill and wing lengths declined according to historical scaling relationships, which could be a consequence of nutritional stress during development or a shift in the proportion of birds from smaller-sized, western breeding populations. Except for juvenile semipalmated sandpipers, we did not find evidence for an increase in the proportion of birds from different breeding populations at the stopover site. Given the wide, hemispheric distribution of these sandpipers throughout their annual cycles, our results, paired with those from a previous study, provide evidence for wide-spread reduction in wing lengths of Calidridine sandpipers since the 1980s. The shorter wing lengths and more convex wing shapes found in this study support the hypothesis that selection has favored more maneuverable wing morphology in small sandpipers.

Wing morphing allows gulls to modulate static pitch stability during gliding.

A gliding bird's ability to stabilize its flight path is as critical as its ability to produce sufficient lift. In flight, birds often morph the shape of their wings, but the consequences of avian wing morphing on flight stability are not well understood. Here, we investigate how morphing the gull elbow joint in gliding flight affects their static pitch stability. First, we combined observations of freely gliding gulls and measurements from gull wing cadavers to identify the wing configurations used during gliding flight. These measurements revealed that, as wind speed and gusts increased, gulls flexed their elbows to adopt wing shapes characterized by increased spanwise camber. To determine the static pitch stability characteristics of these wing shapes, we prepared gull wings over the anatomical elbow range and measured the developed pitching moments in a wind tunnel. Wings prepared with extended elbow angles had low spanwise camber and high passive stability, meaning that mild perturbations could be negated without active control. Wings with flexed elbow angles had increased spanwise camber and reduced static pitch stability. Collectively, these results demonstrate that gliding gulls can transition across a broad range of static pitch stability characteristics using the motion of a single joint angle.

Morphometry of pectoral muscle fiber and intestinal villi of Calidris pusilla during the wintering period in Brazil / Morfometria da fibra muscular peitoral e das vilosidades intestinais de Calidris pusilla durante o período de invernada no Brasil

Migration is an event observed in several animals, such as shorebirds moving between the northern and southern hemispheres, during breeding and wintering intervals. Morphophysiological adaptations are necessary to allow the maintenance of migratory cycles and, therefore, studies with this focus can help clarify biological aspects related to migration. We analyzed the morphology variation in pectoral muscles and intestinal mucosa of Calidris pusilla, during different phases of the wintering period on the coast of Brazil. Fragments of pectoral muscles and duodenal were collected, fixed and processed for histology according to standard procedure, from specimens captured in a locality on the Brazilian coast. Modifications were found in the measured parameters among the three phases of wintering, arrival in Brazil (October, mid-period), January and departure to the Northern Hemisphere - May. The registered structural dynamism characterizes the growth of flight musculature and intestinal changes related to nutrition. Such changes occur temporarily due to the activities of preparation and migration between the northern and southern hemispheres.(AU)

A migração é um evento observado em vários animais, como as aves limícolas que se deslocam entre os hemisférios norte e sul, durante os intervalos de reprodução e invernada. Adaptações morfofisiológicas são necessárias para permitir a manutenção dos ciclos migratórios e, portanto, estudos com esse enfoque podem ajudar a esclarecer aspectos biológicos relacionados à migração. Analisamos a variação morfológica nos músculos peitorais e mucosa intestinal de Calidris pusilla, durante diferentes fases do período de invernada no litoral brasileiro. Fragmentos de músculos peitorais e duodenais foram coletados, fixados e processados ​​para histologia de acordo com o procedimento padrão, a partir de espécimes capturados na localidade da costa brasileira. O dinamismo estrutural registrado caracteriza o crescimento da musculatura de vôo e as alterações intestinais relacionadas à nutrição. As mudanças nos parâmetros medidos entre as três fases do inverno, chegada ao Brasil (outubro, meio período), janeiro e saída para o Hemisfério Norte. Tais mudanças ocorrem temporariamente devido às atividades de preparação e migração entre os hemisférios norte e sul.(AU)

How the egg rolls: a morphological analysis of avian egg shape in the context of displacement dynamics.

Very little is known about how morphology affects the motion, spatial stability and resulting viability of avian eggs. The limited existing research focuses on the uniquely pyriform egg shapes found in the Alcidae bird family. This unusual shell shape was originally thought to suppress displacement and prevent egg loss on the cliffside nesting habitat of the Uria genus. Unfortunately, these early studies never isolated or quantified the specific morphological features (elongation, asymmetry and conicality) of these pyriform eggs, which limits their applicability to other taxa and has hampered a robust proof of concept. We isolated each feature as an enumerated variable, produced model 3D printed eggs with incremental expressions of a single variable and then with all three features co-varying simultaneously. Recorded motion (egg-rolling) trials were conducted to test the individual and combined effects of each morphological characteristic on displacement over a range of inclines representative of the conditions found in natural habitats. Increasing elongation and asymmetry significantly increased displacement, whereas increased conicality decreased displacement in the single-variable egg models. In the multivariable egg models, only conicality consistently suppressed displacement, while lower levels of asymmetry significantly increased displacement. Our findings broadly support previous studies' assertions of the adaptive value of the pyriform eggs while also providing methodology and comparative data for future analyses of the interactions between nesting habitat, behavior and egg shape, beyond the confines of a handful of focal species.

The distribution and heterogeneity of mast cells in tongue from five different avian species.

This study was conducted with the aim of determining the morphology, distribution and heterogeneity of mast cells in the tongues of seagull (Larus fuscus), common buzzard (Buteo buteo), goose (Anser anser), white stork (Ciconia ciconia) and Gerze rooster. The study used five samples of tongue material from each of the healthy adult avian species. The samples were fixed in 10% neutral-buffered formalin (NBF) solution, then, after routine tissue follow-up, the samples blocked with paraplast. Cross-sections with 5-6 µm of thickness were stained with the 0.5% toluidine blue and alcian blue/safranin O (AB/SO). In all five avian species, it was found that the mast cells were in different sizes and round, oval or spindle-shaped based on their place of distribution. Mast cell numbers were determined in stained with toluidine blue, examined ×40 objectives in a 1 mm2 area. It was observed that mast cell density in subepithelial lamina propria and microscopic papilla was higher in the tongues of all species. Mast cell distribution and heterogeneity varied through the tongue, and there were more mast cells in the dorsal side of the tongue than the ventral side. The highest amount of mast cells was found in the tongue of the Gerze rooster among all five species. In the tongue cross-sections stained with the combined method of alcian blue/safranin O (AB/SO), the mast cells were stained as AB (+), SO (+) and AB/SO (+) (mixed).

Size and number of the hypoglossal nerve foramina in the avian skull and their potential neuroanatomical significance.

The cranial openings of nervus hypoglossus, the 12th cranial nerve, are for the first time studied across a broad range of higher avian taxa. This nerve plays an important role in the innervation of the syrinx and exits the skull through a variable number of foramina. Most previous authors described 2-3 foramina nervi hypoglossi (FNH) for neornithine birds, but the number, size, and arrangement of FNH is actually more variable than what is apparent from the literature. In the case of three foramina, there is usually a pair of caudal foramina and a rostral one, but even in closely related taxa, a great variability of the FNH pattern may exist. Many taxa of Neognathae exhibit a quadruple of symmetrically arranged FNH, in others four foramina are strung together in a line. A few taxa show more than four FNH, although in these cases the additional foramina are very small. Of particular interest is the occurrence of a very large caudal FNH in Trochilidae and many species of Passeriformes. This large foramen is suggestive of a correlation with the highly developed vocal capabilities of these birds and may transmit fibers from the tracheosyringeal portion of nucleus nervi hypoglossi, in which case it would be an osteological correlate of vocal capabilities. However, targeted neuroanatomical studies are required to determine how individual hypoglossal foramina relate to hypoglossal roots and their branches, and which of them receive fibers supplying axial, lingual, and syringeal muscles.

Macroanatomic, light, and electron microscopic examination of pecten oculi in the seagull (Larus canus).

The present study was conducted to determine macroanatomic characteristic as well as light and electron microscopic examination (SEM) of pecten oculi and totally 20 bulbus oculi belonging to 10 seagulls (Larus canus) were used. Pecten oculi formations consisted of 18 to 21 pleats and their shape looked like a snail. Apical length of the pleats forming pecten oculi were averagely measured as 5.77 ± 0.56 mm, retina-dependent base length was 9.01 ± 1.35 mm and height was measured as 6.4 ± 0.62 mm. In pecten oculi formations which extend up to 1/3 of the bulbus oculi, two different vascular formations were determined according to thickness of the vessel diameter. Among these, vessels with larger diameters which are less than the others in count were classified as afferent and efferent vessels, smaller vessels which are greater in size were classified as capillaries. Furthermore, the granules which were observed intensely in apical side of the pleats of pecten oculi were observed to distribute randomly along the plica.

Physiological, Morphological and Behavioural Responses of Self-Feeding Precocial Chicks Copying with Contrasting Levels of Water Salinity during Development.

Combined physiological and behavioural responses to salt loads during development have rarely been studied in air-breathing vertebrates able to inhabit hypersaline habitats, but they may be of particular importance in understanding, for example, the differences among species in patterns of habitat use or ontogenetic diet switches. Here, we compared the physiological and behavioural responses of self-feeding precocial chicks developed in contrasting levels of water salinity. The model species was the Black-winged Stilt (Himantopus himantopus) a precocial shorebird that breeds in a range of habitats from freshwater to hypersaline wetlands. Specifically, we compared resting metabolic rate (RMR), heat shock proteins (Hsp70), plasma ions, hematocrit, body mass, body size, growth rate and head-shaking behaviour of captive-reared Black-winged Stilt fledglings developed under fresh (0 ‰), saline (20 ‰), and hypersaline (60 ‰) water. Contrary to expectations, none of the physiological and morphological variables measured differed significantly among treatments. Likewise, the RMR of wild and captive-reared fledglings was similar. Surprisingly, the saltgland mass of wild fledglings from freshwater and those from hypersaline habitats was also similar. However, head-shaking, a behavioural response associated to minimize salt intake and to expel the secretions of salt glands, differed according to salinity source: head-shaking rate increased with increasing salinity. The results of this study support the key role of behavioural osmoregulation in avoiding salt stress during development.

A new extinct species of Snipe (Aves: Scolopacidae: Gallinago) from the West Indies.

We describe an extinct species of snipe (Gallinago kakuki, new species) from late Quaternary fossils in the Bahamian Archipelago (Abaco, New Providence, Little Exuma, Long, and Middle Caicos islands). The new species is known as well from fossils on Cuba, and Cayman Brac in the Cayman Islands. This rather large species of snipe was volant, although because of its relatively short carpometacarpus, the primary flight feathers probably were short. The only other species of Gallinago from the West Indies is the extant, migratory G. delicata, which breeds only in North America. Gallinago kakuki shares more osteological characters with two Eurasian species (G. media, G. hardwickii) than with either of the New World species we examined (G. delicata, G. paraguaiae). A possible inter-hemispherical relationship has been proposed as well for the two extinct, late Quaternary species of woodcocks from the West Indies (Scolopax anthonyi of Puerto Rico, S. brachycarpa of Hispaniola).

Morphology and motion: hindlimb proportions and swing phase kinematics in terrestrially locomoting charadriiform birds.

Differing limb proportions in terms of length and mass, as well as differences in mass being concentrated proximally or distally, influence the limb's moment of inertia (MOI), which represents its resistance to being swung. Limb morphology - including limb segment proportions - thus probably has direct relevance for the metabolic cost of swinging the limb during locomotion. However, it remains largely unexplored how differences in limb proportions influence limb kinematics during swing phase. To test whether differences in limb proportions are associated with differences in swing phase kinematics, we collected hindlimb kinematic data from three species of charadriiform birds differing widely in their hindlimb proportions: lapwings, oystercatchers and avocets. Using these three species, we tested for differences in maximum joint flexion, maximum joint extension and range of motion (RoM), in addition to differences in maximum segment angular velocity and excursion. We found that the taxa with greater limb MOI - oystercatchers and avocets - flex their limbs more than lapwings. However, we found no consistent differences in joint extension and RoM among species. Likewise, we found no consistent differences in limb segment angular velocity and excursion, indicating that differences in limb inertia in these three avian species do not necessarily underlie the rate or extent of limb segment movements. The observed increased limb flexion among these taxa with distally heavy limbs resulted in reduced MOI of the limb when compared with a neutral pose. A trade-off between exerting force to actively flex the limb and potential savings by a reduction of MOI is skewed towards reducing the limb's MOI as a result of MOI being in part a function of the radius of gyration squared. Increased limb flexion is a likely means to lower the cost of swinging the limbs.

Microglia and neurons in the hippocampus of migratory sandpipers.

The semipalmated sandpiper Calidris pusilla and the spotted sandpiper Actitis macularia are long- and short-distance migrants, respectively. C. pusilla breeds in the sub-arctic and mid-arctic tundra of Canada and Alaska and winters on the north and east coasts of South America. A. macularia breeds in a broad distribution across most of North America from the treeline to the southern United States. It winters in the southern United States, and Central and South America. The autumn migration route of C. pusilla includes a non-stop flight over the Atlantic Ocean, whereas autumn route of A. macularia is largely over land. Because of this difference in their migratory paths and the visuo-spatial recognition tasks involved, we hypothesized that hippocampal volume and neuronal and glial numbers would differ between these two species. A. macularia did not differ from C. pusilla in the total number of hippocampal neurons, but the species had a larger hippocampal formation and more hippocampal microglia. It remains to be investigated whether these differences indicate interspecies differences or neural specializations associated with different strategies of orientation and navigation.