Avian-like breathing mechanics in maniraptoran dinosaurs

In 1868 Thomas Huxley first proposed that dinosaurs were the direct ancestors of birds and subsequent analyses have identified a suite of 'avian' characteristics in theropod dinosaurs. Ossified uncinate processes are found in most species of extant birds and also occur in extinct non-avian maniraptoran dinosaurs. Their presence in these dinosaurs represents another morphological character linking them to Aves, and further supports the presence of an avian-like air-sac respiratory system in theropod dinosaurs, prior to the evolution of flight. Here we report a phylogenetic analysis of the presence of uncinate processes in Aves and non-avian maniraptoran dinosaurs indicating that these were homologous structures. Furthermore, recent work on Canada geese has demonstrated that uncinate processes are integral to the mechanics of avian ventilation, facilitating both inspiration and expiration. In extant birds, uncinate processes function to increase the mechanical advantage for movements of the ribs and sternum during respiration. Our study presents a mechanism whereby uncinate processes, in conjunction with lateral and ventral movements of the sternum and gastral basket, affected avian-like breathing mechanics in extinct non-avian maniraptoran dinosaurs.     

Ventilatory mechanics from maniraptoran theropods to extant birds

Shared behavioural, morphological and physiological characteristics are indicative of the evolution of extant birds from nonavian maniraptoran dinosaurs. One such shared character is the presence of uncinate processes and respiratory structures in extant birds. Recent research has suggested a respiratory role for these processes found in oviraptorid and dromaeosaurid dinosaurs. By measuring the geometry of fossil rib cage morphology, we demonstrate that the mechanical advantage, conferred by uncinate processes, for movements of the ribs in the oviraptorid theropod dinosaur, Citipati osmolskae, basal avialan species Zhongjianornis yangi, Confuciusornis sanctus and the more derived ornithurine Yixianornis grabaui, is of the same magnitude as found in extant birds. These skeletal characteristics provide further evidence of a flow-through respiratory system in nonavian theropod dinosaurs and basal avialans, and indicate that uncinate processes are a key adaptation facilitating the ventilation of a lung air sac system that diverged earlier than extant birds.     

Supply-Side Constraints Are Insufficient to Explain the Ontogenetic Scaling of Metabolic Rate in the Tobacco Hornworm,Manduca sexta

Explanations for the hypoallometric scaling of metabolic rate through ontogeny generally fall into two categories: supply-side constraints on delivery of oxygen, or decreased mass-specific intrinsic demand for oxygen. In many animals, supply and demand increase together as the body grows, thus making it impossible to tease apart the relative contributions of changing supply and demand to the observed scaling of metabolic rate. In larval insects, the large components of the tracheal system are set in size at each molt, but then remain constant in size until the next molt. Larvae of Manduca sexta increase up to ten-fold in mass between molts, leading to increased oxygen need without a concomitant increase in supply. At the molt, the tracheal system is shed and replaced with a new, larger one. Due to this discontinuous growth of the tracheal system, insect larvae present an ideal system in which to examine the relative contributions of supply and demand of oxygen to the ontogenetic scaling of metabolic rate. We observed that the metabolic rate at the beginning of successive instars scales hypoallometrically. This decrease in specific intrinsic demand could be due to a decrease in the proportion of highly metabolically active tissues (the midgut) or to a decrease in mitochondrial activity in individual cells. We found that decreased intrinsic demand, mediated by a decrease in the proportion of highly metabolically active tissues in the fifth instar, along with a decrease in the specific mitochondrial activity, contribute to the hypoallometric scaling of metabolic rate.     

Effect of respiratory muscle tension on lung volume.

The chest wall is modeled as a linear system for which the displacements of points on the chest wall are proportional to the forces that act on the chest wall, namely, airway opening pressure and active tension in the respiratory muscles. A standard theorem of mechanics, the Maxwell reciprocity theorem, is invoked to show that the effect of active muscle tension on lung volume, or airway pressure if the airway is closed, is proportional to the change of muscle length in the relaxation maneuver. This relation was tested experimentally. The shortening of the cranial-caudal distance between a rib pair and the sternum was measured during a relaxation maneuver. These data were used to predict the respiratory effect of forces applied to the ribs and sternum. To test this prediction, a cranial force was applied to the rib pair and a caudal force was applied to the sternum, simulating the forces applied by active tension in the parasternal intercostal muscles. The change in airway pressure, with lung volume held constant, was measured. The measured change in airway pressure agreed well with the prediction. In some dogs, nonlinear deviations from the linear prediction occurred at higher loads. The model and the theorem offer the promise that existing data on the configuration of the chest wall during the relaxation maneuver can be used to compute the mechanical advantage of the respiratory muscles.     

Thermal and oxygen conditions during development cause common rough woodlice (Porcellio scaber) to alter the size of their gas-exchange organs

Terrestrial isopods have evolved pleopodal lungs that provide access to the rich aerial supply of oxygen. However, isopods occupy conditions with wide and unpredictable thermal and oxygen gradients, suggesting that they might have evolved adaptive developmental plasticity in their respiratory organs to help meet metabolic demand over a wide range of oxygen conditions.To explore this plasticity, we conducted an experiment in which we reared common rough woodlice (Porcellio scaber) from eggs to maturation at different temperatures (15 and 22 °C) combined with different oxygen levels (10% and 22% O₂). We sampled animals during development (only females) and then examined mature adults (both sexes). We compared woodlice between treatments with respect to the area of their pleopod exopodites (our proxy of lung size) and the shape of Bertalanffy’s equations (our proxy of individual growth curves).Generally, males exhibited larger lungs than females relative to body size. Woodlice also grew relatively fast but achieved a decreased asymptotic body mass in response to warm conditions; the oxygen did not affect growth. Under hypoxia, growing females developed larger lungs compared to under normoxia, but only in the late stage of development. Among mature animals, this effect was present only in males. Woodlice reared under warm conditions had relatively small lungs, in both developing females (the effect was increased in relatively large females) and among mature males and females.Our results demonstrated that woodlice exhibit phenotypic plasticity in their lung size. We suggest that this plasticity helps woodlice equilibrate their gas exchange capacity to differences in the oxygen supply and metabolic demand along environmental temperature and oxygen gradients. The complex pattern of plasticity might indicate the effects of a balance between water conservation and oxygen uptake, which would be especially pronounced in mature females that need to generate an aqueous environment inside their brood pouch.     

Body condition of a small passerine bird: ultrasonic assessment and significance in overwinter survival

The fitness benefits of intraspecific variation in physiological attributes have rarely been measured. Body condition, defined as the current status of metabolic reserves relative to likely demands, has often been implicated in subsequent survival, but has proved difficult to assess reliably in the live animal. A technique for assessing body condition, in terms of the main protein reserve of small birds, is presented. Pectoralis muscle thickness was measured in live birds using ultrasound reflection from the sternum. The relationship between the relative size of pectoralis muscles in autumn and the likelihood of overwinter survival in the dipper Cinclus cinclus was examined. The pectoralis reserves of male dippers surviving overwinter were significantly greater than those of birds which died or disappeared between late November and the breeding season in April. In contrast, variation in autumn condition of females was unrelated to overwinter survival.     

Intercostal muscle action inferred from finite-element analysis

The external and internal intercostal muscles are important respiratory muscles in humans, but their mechanical actions have been controversial. We used finite-element analysis based on anatomic and mechanical measurements in dogs to assess the action of the intercostal and other rib cage muscles in a model of an isolated canine rib cage. When intercostal muscle forces of either the internal or the external layer were applied in a single interspace, they pulled the adjacent ribs together, consistent with published observations in dogs. However, when the forces were applied in all interspaces, the external layer caused an inspiratory motion and the internal layer caused an expiratory motion, consistent with conventional understanding of intercostal muscle actions. Parasternal intercostal, levator costae, and transversus thoracis (triangularis sterni) muscle actions were also simulated. These muscles caused expected movements of the ribs and sternum. We conclude that the actions of intercostal muscles depend on the spatial extent of their activation. Their actions in a single interspace and in multiple interspaces can be observed and explained with three-dimensional finite-element models.     

Relationships Among Powered Flight,Metabolic Rate,Body Mass,Genome Size,and the Retrotransposon Complement of Volant Birds

Avian genomes are of interest because the rapid metabolic rate associated with powered flight requires small cells which constrain genome size. Consequently, flying birds tend to have small genomes relative to other vertebrates such as mammals. It thus stands to reason that flying birds should have smaller genomes than ground-dwelling birds with lower metabolic rates. Small genomes could be condensed but uncompromised in a number of ways, including smaller intergenic intervals, shorter introns, and/or a reduced transposable element (TE) complement. We evaluated genome size in light of the orthologous TE complement among 41 flying (FY) and seven ground-dwelling (GD) bird species to determine if a preponderance of deletions in orthologous TEs might explain the compact genomes of flying birds with high metabolic rates. We measured, across multiple loci in all 48 species, the lengths of 50 contemporary orthologous chicken repeat 1 (CR1, a non-LTR retrotransposon) copies relative to inferred ancestral CR1 sequences. We found genome sizes in GD birds were not different than those in FY birds, but the mean lengths of orthologous CR1 loci were significantly shorter in FY birds than in GD birds. Moreover, we observed a negative correlation between basal metabolic rate and length of orthologous CR1 loci. Finally, we observed positive correlations between body mass and both genome sizes as well as length of orthologous CR1 loci, which we expected given that body mass correlates negatively with metabolic rates. Our results support the contention that metabolism helps shape the avian TE complement and thus indirectly contributes to the compact genomes of birds.     

Der Atemapparat der V?gel und ihre lokomotorische und metabolische Leistungsf?higkeit

Zusammenfassung Zum Verständnis der besonderen Struktur- und Funktionsprinzipien des Atemapparates der Vögel werden die spezielle Bauweise des Vogelrumpfes und die bei den Vögeln hochdifferenzierte Septierung ihrer Leibeshöhle dargestellt. Sodann werden der Bau der Lungen und ihres Bronchialsystems beschrieben sowie die Lage und Verbindungen der Luftsäcke und ihrer Divertikel. Die Schilderung der Atembewegungen des Vogelrumpfes ergibt die Grundlage für die Diskussion der Ventilation der Vogellunge. Auf die Darstellung des Aufbaus der Parabronchien, der funktionellen Baueinheit für den Gasaustausch in der Vogellunge, sowie ihres Gefäßsystems folgen die Daten über den quantitativen Aufbau des Lungen-Luftsacksystems von Kolibris bis zu Schwänen und ihrer morphometrisch bestimmten Austauschkapazitäten. Anschließend werden die physiologischen Daten über den Gasaustausch in der Vogellunge und den Transport der Atemgase durch das Blut diskutiert und die Kenntnisse über die sensorische und neuronale Steuerung von Atmung und Gasaustausch aufgeführt. Sodann werden die vorhandenen Daten über den qualitativen und quantitativen Aufbau der Flugmuskulatur und des Herz-Kreislaufsystems zusammengestellt und ihre körpergrößenabhängigen Beziehungen und deren funktionelle Konsequenzen diskutiert. Abschließend wird die Evolution der Vögel als hochentwickelter Warmblüter diskutiert, die mit ihren zu Dauerleistung befähigten Schlagfliegern wie vielen Zugvögeln extrem gesteigerte metabolische und lokomotorische Leistungen vollbringen, von denen sich die als Bodenvögel spezialisierten größeren Hühnervögel mit ihrer sehr beschränkten physiologischen Leistungsfähigkeit aber deutlich unterscheiden.

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The respiratory apparatus of birds and their locomotory and metabolic efficiency

Summary The structural and functional principles of the avian respiratory apparatus and the differences with respect to the respiratory apparatus of mammals have been well understood from published investigations since 1970 (for review articles see Duncker 1971, 1978a, 1979, 1983, Fedde 1986, Seller 1987, King & McLelland 1989). The various and great structural and functional differences between birds and mammals are often ignored or have only rarely found adequate treatment. In the face of the fundamental structural uniformity of birds, the large differences which exist in the functional efficiency of their respiratory and cardiovascular apparatus are not generally realized. This applies to an even greater extent to their interaction and cooperation with the locomotory apparatus, especially when comparing the well-known domestic fowl with the more rarely examined wild and migratory birds. Migratory birds are vertebrates whose respiratory, cardiovascular und locomotory apparatus are capable of the highest sustainable effort. In contrast, the physiology of larger fowl-like birds is not designed for the purpose of hard and sustained exercise, but in accordance with their anaerobically performed short escape flight, the capacity of their cardiovascular and respiratory systems is greatly reduced. Fowl-like birds are therefore suitable only to a very limited extent to afford a functional understanding of avian construction. With this in mind the present article reviews the structure of the respiratory apparatus of birds with its important qualitative and quantitative structural and functional characteristics and the functionally important and correlated aspects of the cardiovascular and locomotory systems. Against this background these avian systems are compared with the functional characteristics of the corresponding mammalian systems.The lung air sac system of birds is related to the special construction of the avian trunk and the highly differentiated septation of the body cavity of birds (Fig. 1; Duncker 1971, 1979). The construction of the trunk wall and the septation of the body cavity are responsible for the volume constancy of the pleural cavity during all respiratory movements, thus establishing the necessary structural conditions for the development of the rigid parabronchial lung. Only under these conditions can the parabronchial air capillaries remain extended and air-filled. The ventilation of this rigid avian lung is achieved by the volume changes of the air sacs, whereby the air flow through the parabronchi is directed aerodynamically. The relative rigidity of the avian trunk with its highly specialized articulations between the spinal column, which is more or less immobile, and the ribs and the sternum enables large excursions for the breathing movements so that ventilation of the air sacs can occur with a large amplitude and at minimum pressure differences. By virtue of the large volume elasticity (compliance) of the air sacs the respiratory apparatus of birds works as a low-pressure system. In addition, owing to the special construction of the shoulder girdle of birds as well as to the arrangement of the large flight muscles and the air sac diverticula between the cranial shoulder girdle and the frontal thorax, complete dissociation of respiratory and flight movements can result, which allows birds to fly and to breath with different, even changing frequencies, which are related specifically to body size (Fig. 5; Berger & Hart 1974).In contrast to this avian construction, the mammalian trunk, especially in small to mediumsized mammals, possesses a strongly elastic thorax and a highly pliant lumbar vertebral column, which result in a coupling between locomotory and respiratory movements. The thoracic cage and the cervical and thoracic vertebral column represent the crucial origins for the musculature of the shoulder girdle including its highly mobile scapula. The extensive movements of the lumbar vertebral column are substantial for the locomotory movements of the hind limb. Owing to its small volume elasticity (compliance) and powerful retractile forces, the broncho-alveolar mammalian lung requires larger pressure gradients for full inspiration. Thus, the thorax musculature and a muscularized diaphragm are well developed. In addition to the performance of its inspiratory movements, the diaphragm must also counteract the high intraabdominal pressures, which are an inevitable consequence of the extensive movements of the lumbar vertebral column and the active abdominal muscles, especially during rapid locomotion. Thus, the body cavities of mammals including the pleural cavity are high-pressure systems, which have multiple, not yet investigated effects on the structure and function of different organ systems.Just as the structure and function of the lung air sac apparatus of birds differ fundamentally from the lungs of mammals, the ontogenetic development of the respiratory apparatuses of these two classes are also basically different. In viviparous mammals the lung develops similarly to all lungs of amniotes secreting pulmonary fluid, which fills the lumina of the developing bronchial tree including its respiratory portion. With the onset of respiratory movements in the late embryological/fetal development, this pulmonary fluid comes into partial exchange with the amniotic fluid. During parturition, a portion of the pulmonary fluid is squeezed out by the compression of the fetus. The remaining pulmonary fluid, which is sucked into the terminal ends of the respiratory bronchial tree by the first breath, will be resorbed in the first few hours of life by active transport of the alveolar epithelium and the endothelium of the alveolar capillaries. Thus, the mammalian lung, which has developed a thin exchange surface in the sacculi or alveoli of the respiratory bronchial tree, can aerate most of the exchange surface with the first breath at birth so that it can instantly take over the function of gas exchange from the placenta (Duncker 1990).The avian lung and its principal air sacs develop in the embryo, which is emersed in the amniotic fluid of the egg. Similarly, the lumina of the growing bronchial system are filled with pulmonary fluid. Towards the end of the incubation period the air capillaries start to sprout from the tubuli of the fluid-filled anlagen of the parabronchi between the surrounding blood capillaries. One to three days before hatching, after having swallowed the remaining amniotic fluid, and initiated regular breathing movements, the chick perforates the membrane into the air chamber of the egg (Duncker 1978b, Piiper 1978). Thus, not only the primary and secondary bronchi of the lung and the large air sacs are ventilated, but also the lumina of the parabronchi. The parabronchial air capillaries, which continue growing and sprouting, are filled with pulmonary fluid, which is now absorbed by the epithelium of the air capillaries and the endothelium of the blood capillaries. Depending upon the size of the egg and the duration of the incubation, the air capillaries are completely air-filled after one to two days. With this ventilation and the increasing filling of the air capillaries with air, they progressively assume the gas exchange function, which up to this time has been carried out by the chorioallantoic membrane. The latter is closely attached to the inside of the shell membrane. At the end of this process the embryo hatches. As early as in the embryological development the pleural cavities maintain volume constancy during all respiratory and body movements. The rigid lungs, which grow together with the pleural cavity walls during their embryological development, attain their gas exchange ability after ventilation of the bronchial system only through the resorption of the pulmonary fluid by the epithelium of the air capillaries. The avian lung therefore can only attain its functional capacity for gas exchange by a temporal overlapping of gas exchange by the chorioallantoic membrane with the respiration of air by the lung, which is only possible in a hard-shelled egg. Thus, the highly differentiated, non-inflatable lung structure in birds is inevitably bound to development in a hard-shelled egg (Duncker 1978b).All birds possess a respiratory apparatus that in principle is comparably constructed. They differ vastly, however, in the extent to which the diffusion capacity of their lungs is developed and thus in their metabolic and locomotory efficiency. Those capable of sustained, efficient flight, e.g. hummingbirds to large migratory birds, possess lungs with an exchange capacity that is higher than that of comparably large mammals by a factor of 6 to 8 (Fig. 27). The relative weight of the heart of birds and their cardio-vascular transport capacity are correspondingly larger than in comparable mammals and they have a somewhat larger relative blood volume (Duncker & Güntert 1985). By virtue of this construction, sustainably flying birds can supply their flight musculature, which consists to a large extent or completely of aerobic muscle fibers, which are sufficient for a continuous flapping type flight activity. However, a crucial body-size relationship arises within these functional interdependencies, since the hearts of larger animals can only pump a relatively smaller blood volume per time unit owing to the size-dependent maximum pulse rate. Accordingly, large ducks, geese and swans adapt to these scale problems by a reduction in their relative flight muscle mass, which entailes them using a longer time for take-off with violent flapping of their wings (Fig. 28). Large water birds can perform such a long take-off only on water, out of reach of preying terrestrial hunters.Large land birds, like the large fowl-like birds, owe their survival to the fact that they can save themselves from stalking hunters by a direct lifting flight, in order to escape into a tree or by sweeping off to a safe distance. For a direct lifting flight, however, a flight muscle mass of at least 20% of their total body weight is necessary. Larger sustainably flying birds had to reduce their aerobic, red flight musculature to 13–12% of their total body mass in accordance with the described body-size dependent cardio-vascular blood transport capacity. Based on these scaling interdependencies, the medium- to large-sized fowl-like birds could not differentiate aerobic fibers in their flight musculature. Because of the requirement that flight musculature must amount to 20% of body weight for lifting stroke flight, they were able to differentiate their flight muscles only as anaerobic, white fibers and thus they can fly strongly but fatigue very quickly (Fig. 28). Accordingly, the heart and circulatory system has also differentiated to the physiological needs of the flight musculature. Thus, the size of the heart and the cardio-vascular transport capacity of larger fowl-like birds are reduced to half of or less than the heart size and transport capacity of comparably large sustainably flying birds, and they possess an even more greatly reduced diffusion capacity of their lungs. Medium-sized and large fowl-like birds passed up the development of the ability for sustainable higher metabolic permormance during their very special evolution towards a more terrestrially based, running bird with short escape flight. The fowl-like birds, adapted very well to their specific habitat, therefore are not an appropiate example of a typical bird with the ability for long-term, flapping flight and high metabolic achievement.

     

Triangularis sterni: a primary muscle of breathing in the dog

The isolated action, pattern of neural activation, and mechanical contribution to eupnea of the triangularis sterni (transversus thoracis) muscle were studied in supine anesthetized dogs. Linear displacement transducers were used to measure the axial displacements of the ribs and sternum. Tetanic stimulation of the triangularis sterni in the apneic animal caused a marked caudal displacement of the ribs, a moderate cranial displacement of the sternum, and a decrease in lung volume. During quiet breathing, there was invariably a rhythmic activation of the muscle in phase with expiration that was independent of the presence or absence of activity in the abdominal and internal interosseous intercostal muscles. This phasic expiratory activity in the triangularis sterni was of large amplitude and caused the ribs to be more caudal and the sternum to be more cranial during the spontaneous expiratory pause than during relaxation. Additional studies on awake animals showed that rhythmic activation of the triangularis sterni occurs in all body positions and is not caused by anesthesia. These findings indicate that expiration in the dog is not a passive process and that the end-expiratory volume of the rib cage is not determined by an equilibrium of static forces alone. Rather, it is actively determined and maintained below its relaxation volume by contraction of the triangularis sterni throughout expiration. The use of this muscle is likely to facilitate inspiration by increasing the length of the parasternal intercostals and taking on a portion of their work.     

Changes in chest wall structure and elasticity in elastase-induced emphysema

The present study examined the effects of elastase-induced emphysema on the structure and elasticity of the chest wall. Specifically, we examined the passive pressure-volume relationship of the intact chest wall in anesthetized animals and the stress-strain relationship of the isolated rib cage devoid of respiratory musculature. The structure of the isolated rib cage was assessed by measuring its circumferential, anterior-posterior, and transverse dimensions, the angles of articulation of the ribs at the costovertebral and sternochondral joints, and the length of the sternum and individual ribs. Studies were performed in 10 Syrian Golden hamsters, 26-27 wk after intratracheal injection of elastase, and 9 saline-injected hamsters that served as controls. Mean functional residual capacity of emphysematous animals was 239% of the value obtained in control animals. In emphysematous animals, the pressure-volume curve of the chest wall was shifted parallel and to the left of the curve obtained in controls. That is, at any given esophageal pressure, lung volume was significantly greater in emphysematous animals compared with controls, but the slope of the pressure-volume relationship was similar in the two groups. In the relaxed position, the circumference, anterior-posterior, transverse, and rostral-caudal dimensions of the thorax were significantly greater in emphysematous than control animals. Although the length of the thoracic spinal column was the same in both groups, the length of the ribs and sternum were greater in emphysematous animals and the angles of articulation of the ribs with the vertebrae and sternum were altered.(ABSTRACT TRUNCATED AT 250 WORDS)     

Energetics of fattening and starvation in the long-distance migratory garden warbler,Sylvia borin,during the migratory phase

Garden warblers (Sylvia borin) were subjected to starvation trials during their autumnal migratory phase in order to simulate a period of non-stop migration. Before, during and after this treatment the energy expenditure, activity, food intake and body mass of the subjects were monitored. Assimilation efficiency was constant throughout the experiments. The catabolized (during starvation) and deposited body tissue (during recovery) consisted of 73% fat. Basal metabolic rate was decreased during the starvation period and tended to a gradual increase during the recovery period. The reduced basal metabolic rate can possibly be attributed to a reduced size/function of the digestive system, which is consistent with the sub-maximal food intake immediately after resuming the supply of food to the experimental birds. The observed reductions in basal metabolic rate during starvation and activity during recovery can be viewed as adaptations contributing to a higher economization of energy supplies. The experimental birds were unable to eat large quantities of food directly after a period of starvation leading to a comparatively low, or no increase in body mass. Such a slow mass increase is in agreement with observations of migratory birds on arrival at stop-over sites.Abbreviations BM body mass - BMR basal metabolic rate - LBM lean body mass - RQ respiratory quotient     

The effects of tracheal coiling on the vocalizations of cranes (Aves; Gruidae)

Summary It is generally supposed that the elongated, often coiled tracheae of many species of birds are adaptations for the production of loud, penetrating calls. A corollary supposition is that the acoustic effects are produced by the resonant properties of the elongated tube, with the birds being analogized to a wind instrument. We have experimented with several species of cranes possessing different degrees of tracheal coiling. Regardless of the degree of coiling, all cranes can utter extremely loud calls using remarkably low driving pressures. Neither surgical modifications of the trachea nor changing the respiratory gases to helium-oxygen produced consistent changes of voice that could be unambiguously attributed to changes of tubal resonances. However, shortening the trachea markedly reduced vocal intensity, the degree of reduction being roughly proportional to the degree of shortening. Although some of that reduction may derive from an increased impedance mismatch at the external aperture of the tube, and some from a decreased radiation directly from the hard walls of the trachea, these explanations scarcely account for the dramatic effects we observed. We, therefore, hypothesize a more unusual mechanism: The tracheal coils that are embedded in the sternum serve a function analogous to the bridge of a stringed instrument, transmitting the vibrations of a tiny sound source to a large radiating surface, the sternum. The sternum then vibrates against the large internal air reservoir of the avian airsac system. As it has a complex shape, the sternum will have many resonances and will respond to many frequencies; as a solid oscillator, its resonances will not be greatly affected by low density gases. Hence, we suggest that cranes and other birds with enlarged windpipes are more properly analogized with a violin than a trombone.     

Diet shift induced rapid evolution of size and function in a predatory bird

A predator’s body size correlates with its prey size. Change in the diet may call for changes in the hunting mode and traits determining hunting success. We explored long-term trends in sternum size and shape in the northern goshawk by applying geometric morphometrics. Tetraonids, the primary prey of the goshawk, have decreased and been replaced by smaller birds in the diet. We expected that the size of the goshawk has decreased accordingly more in males than females based on earlier observations of outer morphology. We also expected changes in sternum shape as a function of changes in hunting mode. Size of both sexes has decreased during the preceding decades (1962?2008), seemingly reflecting a shift in prey size and hunting mode. Female goshawks hunting also mammalian prey tend to have a pronouncedly “Buteo-type” sternum compared to males preying upon birds. Interestingly, the shrinkage of body size resulted in an increasingly “Buteo-type” sternum in both sexes. In addition, the sternum shape in birds that died accidentally (i.e., fit individuals) was more Buteo-type than in starved ones, hinting that selection was towards a Buteo-type sternum shape. We conclude that these observed patterns are likely due to directional selection driven by changes in the diet towards smaller and more agile prey. On the other hand, global warming is predicted to also cause a decrease in size, thus these two scenarios are inseparable. Because of difficulties in studying fitness-related phenotypic changes of large raptors in the field, time series of museum exemplars collected over a wide geographical area may give answers to this conundrum.     

Flight costs of long,sexually selected tails in hummingbirds

The elongated tails adorning many male birds have traditionally been thought to degrade flight performance by increasing body drag. However, aerodynamic interactions between the body and tail can be substantial in some contexts, and a short tail may actually reduce rather than increase overall drag. To test how tail length affects flight performance, we manipulated the tails of Anna''s hummingbirds (Calypte anna) by increasing their length with the greatly elongated tail streamers of the red-billed streamertail (Trochilus polytmus) and reducing their length by removing first the rectrices and then the entire tail (i.e. all rectrices and tail covert feathers). Flight performance was measured in a wind tunnel by measuring (i) the maximum forward speed at which the birds could fly and (ii) the metabolic cost of flight while flying at airspeeds from 0 to 14 m s⁻¹. We found a significant interaction effect between tail treatment and airspeed: an elongated tail increased the metabolic cost of flight by up to 11 per cent, and this effect was strongest at higher flight speeds. Maximum flight speed was concomitantly reduced by 3.4 per cent. Also, removing the entire tail decreased maximum flight speed by 2 per cent, suggesting beneficial aerodynamic effects for tails of normal length. The effects of elongation are thus subtle and airspeed-specific, suggesting that diversity in avian tail morphology is associated with only modest flight costs.     

HOW MAMMALS PRODUCE LARGE-BRAINED OFFSPRING

Two explanations for species differences in neonatal brain size in eutherian mammals relate the size of the brain at birth to maternal metabolic rate. Martin (1981, 1983) argued that maternal basal metabolic rate puts an upper bound on the mother's ability to supply energy to the fetus, thereby limiting neonatal brain size. Hofman (1983) proposed that gestation length in mammals is constrained by maternal metabolic rate, implying an indirect constraint on neonatal brain size. Since individuals of precocial species have much larger neonatal brain sizes and are gestated longer for a given maternal body size than individuals of altricial species, Martin's and Hofman's ideas also require that mothers of precocial offspring have higher metabolic rates for their body sizes than mothers of altricial offspring. Data on 116 mammal species from 13 orders show that neither neonatal brain size nor gestation length is correlated with maternal metabolic rate when maternal body-size effects are removed. For a given maternal size, there is no difference in metabolic rates between precocial and altricial species, despite a two-fold difference between them in average neonatal brain size. However, neonatal brain size is strongly correlated with gestation length and litter size, independently of maternal size and metabolic rate. Analyses conducted within orders replicated the findings for gestation length and suggested that neonatal brain size may be at best only weakly related to metabolic rate. Differences in neonatal brain size appear to have evolved primarily with species differences in gestation length and litter size but not with differences in metabolic rate; large-brained offspring are typically produced from litters of one that have been gestated for a long time relative to maternal size. We conclude that species differences in relative neonatal brain size reflect different life-history tactics rather than constraints imposed by metabolic rate.     

Effects of thermal and oxygen conditions during development on cell size in the common rough woodlice Porcellio scaber

During development, cells may adjust their size to balance between the tissue metabolic demand and the oxygen and resource supply: Small cells may effectively absorb oxygen and nutrients, but the relatively large area of the plasma membrane requires costly maintenance. Consequently, warm and hypoxic environments should favor ectotherms with small cells to meet increased metabolic demand by oxygen supply. To test these predictions, we compared cell size (hindgut epithelium, hepatopancreas B cells, ommatidia) in common rough woodlice (Porcellio scaber) that were developed under four developmental conditions designated by two temperatures (15 or 22°C) and two air O₂ concentrations (10% or 22%). To test whether small‐cell woodlice cope better under increased metabolic demand, the CO₂ production of each woodlouse was measured under cold, normoxic conditions and under warm, hypoxic conditions, and the magnitude of metabolic increase (MMI) was calculated. Cell sizes were highly intercorrelated, indicative of organism‐wide mechanisms of cell cycle control. Cell size differences among woodlice were largely linked with body size changes (larger cells in larger woodlice) and to a lesser degree with oxygen conditions (development of smaller cells under hypoxia), but not with temperature. Developmental conditions did not affect MMI, and contrary to predictions, large woodlice with large cells showed higher MMI than small woodlice with small cells. We also observed complex patterns of sexual difference in the size of hepatopancreatic cells and the size and number of ommatidia, which are indicative of sex differences in reproductive biology. We conclude that existing theories about the adaptiveness of cell size do not satisfactorily explain the patterns in cell size and metabolic performance observed here in P. scaber. Thus, future studies addressing physiological effects of cell size variance should simultaneously consider different organismal elements that can be involved in sustaining the metabolic demands of tissue, such as the characteristics of gas‐exchange organs and O₂‐binding proteins.     

Buoyancy under Control: Underwater Locomotor Performance in a Deep Diving Seabird Suggests Respiratory Strategies for Reducing Foraging Effort

Background

Because they have air stored in many body compartments, diving seabirds are expected to exhibit efficient behavioural strategies for reducing costs related to buoyancy control. We study the underwater locomotor activity of a deep-diving species from the Cormorant family (Kerguelen shag) and report locomotor adjustments to the change of buoyancy with depth.

Methodology/Principal Findings

Using accelerometers, we show that during both the descent and ascent phases of dives, shags modelled their acceleration and stroking activity on the natural variation of buoyancy with depth. For example, during the descent phase, birds increased swim speed with depth. But in parallel, and with a decay constant similar to the one in the equation explaining the decrease of buoyancy with depth, they decreased foot-stroke frequency exponentially, a behaviour that enables birds to reduce oxygen consumption. During ascent, birds also reduced locomotor cost by ascending passively. We considered the depth at which they started gliding as a proxy to their depth of neutral buoyancy. This depth increased with maximum dive depth. As an explanation for this, we propose that shags adjust their buoyancy to depth by varying the amount of respiratory air they dive with.

Conclusions/Significance

Calculations based on known values of stored body oxygen volumes and on deep-diving metabolic rates in avian divers suggest that the variations of volume of respiratory oxygen associated with a respiration mediated buoyancy control only influence aerobic dive duration moderately. Therefore, we propose that an advantage in cormorants - as in other families of diving seabirds - of respiratory air volume adjustment upon diving could be related less to increasing time of submergence, through an increased volume of body oxygen stores, than to reducing the locomotor costs of buoyancy control.     

A developmental constraint on the fledging time of birds

We examined the hypothesis that the rate of bone growth limits the minimum fledging time of birds. Previous observations in California gulls indicate that linear growth of wing bones may be the rate limiting factor in wing development. If bone growth is rate limiting, then birds with relatively long bones for their size could be expected to have longer fledging periods than birds with relatively short bones. We tested this by comparing the length of wing bones, relative to body mass, to the relative length of fledging periods among 25 families. The results support the hypothesis. A strong correlation exists between relative fledging period and relative bone length. Species which have relatively long bones for their body size tend to take longer to fly. In contrast, parameters that influence flight style and performance, such as size of the pectoralis muscle and wing loading, show little or no correlation with fledging time. The analysis also indicates that, when altricial and precocial species are considered together, bone length is more highly correlated with fledging time than is body mass or rate of increase in body mass during growth. These observations suggest that linear growth of bones does limit the growth of avian wings and that it is one of the factors that influences the fledging time of birds.     

An analysis of possible movements of human upper rib cage

A geometrically realistic mathematical model of the first six ribs and vertebrae of the human rib cage is described. Under the assumption that the individual elements of the rib cage do not deform significantly, the possible range of movements of the model are determined subject to the constraint that the joint surfaces remain in contact. It is shown that normal movements of the ribs cannot be described as a rotation about a single fixed axis. The possible movements of the ribs are analyzed in terms of the misfit incurred at the costovertebral joint surfaces. This analysis shows that there is a movement, corresponding to lateral expansion of the rib for an increase in anteroposterior diameter, in which the misfit at the joint is minimized and also that small deviations from this movement involve only very small degrees of misfit at the joint surfaces. It is concluded that many observed "deformations" of the chest wall can be explained by rigid ribs and normal movements at the costovertebral joints. The interaction between the ribs and the spine is analyzed. It is shown that there can be considerable independent movement of the sternum and the spine, thus allowing mobility of the spine without forcing concomitant movements of rib cage.