A systematic study of the development of the airway (bronchial) system of the avian lung from days 3 to 26 of embryogenesis: a transmission electron microscopic study on the domestic fowl, Gallus gallus variant domesticus

In the embryo of the domestic fowl, Gallus gallus variant domesticus, the lung buds become evident on day 3 of development. After fusing on the ventral midline, the single entity divides into left and right primordial lungs that elongate caudally while diverging and shifting towards the dorsolateral aspects of the coelomic cavity. On reaching their definitive topographical locations, the lungs rotate along a longitudinal axis, attach, and begin to slide into the ribs. First appearing as a solid cord of epithelial cells that runs in the proximal-distal axis of the developing lung, progressively, the intrapulmonary primary bronchus begins to canalize. In quick succession, secondary bronchi sprout from it in a craniocaudal sequence and radiate outwards. On reaching the periphery of the lung, parabronchi (tertiary bronchi) bud from the secondary bronchi and project into the surrounding mesenchymal cell mass. The parabronchi canalize, lengthen, increase in diameter, anastomose, and ultimately connect the secondary bronchi. The luminal aspect of the formative parabronchi is initially lined by a composite epithelium of which the peripheral cells attach onto the basement membrane while the apical ones project prominently into the lumen. The epithelium transforms to a simple columnar type in which the cells connect through arm-like extensions and prominently large intercellular spaces form. The atria are conspicuous on day 15, the infundibulae on day 16, and air capillaries on day 18. At hatching (day 21), the air and blood capillaries have anastomosed profusely and the blood-gas barrier become remarkably thin. The lung is well developed and potentially functionally competent at the end of the embryonic life. Thereafter, at least upto day 26, no further consequential structures form. The mechanisms by which the airways in the avian lung develop fundamentally differ from those that occur in the mammalian one. Compared with the blind-ended bronchial system that inaugurates in the mammalian lung, an elaborate, continuous system of air conduits develops in the avian one. Further studies are necessary to underpin the specific molecular factors and genetic processes that direct the morphogenesis of an exceptionally complex and efficient respiratory organ.     

Do mammals,birds, reptiles and fish have similar nitrogen conserving systems?

Comparative physiological studies are a powerful tool for revealing common animal adaptations. Amino acid catabolism produces ammonia which is detoxified through the synthesis of urea (mammals, some fish), uric acid (birds), or urea and uric acid (reptiles). In mammalian herbivores and omnivores, urea nitrogen is salvaged by a series of steps involving urea transfer into the intestine, microbial mediated urea hydrolysis with synthesis of amino acids utilizing the liberated ammonia and transfer of the amino acids back to the host. A similar series of steps occur in omnivorous/granivorous and herbivorous birds, although in this case urine, containing uric acid, is refluxed directly into the intestine where microbes degrade the uric acid and utilize the liberated ammonia for amino acid synthesis. These amino acids are transferred back to the host. In reptiles and ureotelic fish not all of these steps have been experimentally confirmed. Reptiles like birds, reflux urine into the intestine where it is exposed to the microflora. However, the capacity of these microbes to breakdown the uric acid and urea and utilize ammonia for amino acid synthesis has not been documented. Ureotelic fish transfer urea into the intestine where urease (presumably of bacterial origin) hydrolyzes the urea. However, the amino acid synthesizing capacity of the intestinal microflora has not been studied. The series of steps, as outlined, would define the prevailing nitrogen conservation system for herbivores and omnivores at least. However, it would appear that some animals, in particular the fruit-eating bat and perhaps the fruit-eating bird, may have evolved alternative, as yet uncharacterized, adaptations to a very limited nitrogen intake.     

Broad-scale reciprocity in an avian seed dispersal mutualism

Aim Coevolved relationships between individual species of birds and plants rarely occur in seed dispersal mutualisms. This study evaluates whether reciprocal relationships may occur between assemblages of bird and plant species. Location Vancouver Island, British Columbia, Canada (48°50′‐N, 125°22′‐W). Methods The distribution and fruiting phenologies of seven shrub species were compared to seasonal changes in habitat selection and seed dispersal by six fruit‐eating bird species. Results Shrub species inhabiting forest understorey habitat had earlier fruiting phenologies than shrub species inhabiting forest edge habitat along lake and bog margins. Birds showed a parallel pattern in habitat selection, being more abundant in the forest understorey early in the fruiting season, and more abundant in the forest edge later in the season. Rates of seed deposition covaried with avian habitat selection, in such a way that birds directed seed dispersal into habitats preferred by shrubs. Conclusions These results depict a broad‐scale pattern in the abundance of birds and fruits indicative of reciprocal interactions. Seasonal changes in seed dispersal to each habitat appear to reinforce the relationship between shrub habitat affinities and fruiting phenologies. Phenological differences between habitats may also reinforce seasonal changes in avian habitat selection. Therefore, although reciprocal interactions between pairs of bird and plant species are rare, broad‐scale reciprocal relationships may occur between assemblages of bird and plant species.     

Genome organization and species formation in vertebrates

Some years ago Wilson and co-workers proposed that the higher rates of karyotypic change and species formation of mammals compared to cold-blooded vertebrates are due to the formation of small demes, as favored by the social structuring and brain development of the former. Here, evidence is reviewed which indicates that mammals are more prone to karyotypic change and species formation than cold-blooded vertebrates because of their different genome organization. Similar evidence has also recently become available for birds. While this different organization appears to be a necessary and, in all likelihood, a sufficient condition for the increased rates of karyotypic change and species formation found in mammals, it is still possible that social structuring and brain development may have played an additional accelerating role.This paper was presented at the International Conference on Genome Plasticity held in Cancun, Mexico (December 8–12, 1991)     

Density dependence tests,are they?

A large number of time series of abundances of insects and birds from a variety of data sets were submitted to a new density dependence test. The results varied enormously between data sets, but the relation between the frequency of statistically significant density dependence (SSDD) and the length of the series was similar to that of the power curve of the test, making the results consistent with the hypothesis of the density-dependent model being universally applicable throughout the data used. Pest and non-pest species did not differ in the incidence of SSDD. The more sampling error present in the data, the higher the percentages of SSDD. This was expected given that the power of the test increases with increasing sampling error in the data. Many of the data used here, as well as in the literature, clearly violate the basic assumption of the test that the organism concerned should be univoltine and semelparous. Yet the incidence of SSDD was the same in univoltine as in bi/polyvoltine species and the same in semelparous organisms as in birds that are reproductively active in more than one year. The seasonal migrant Autographa gamma in Britain and Czechoslovakia and even rainfall data were found to have SSDD. Statistical significance, however, does not automatically lead to the conclusion of density-dependent regulation. Any series of random variables which are in a stochastic equilibrium, such as a series of independent, identically distributed, random variables, is typically described better by the alternative (density-dependent) model than by the null (density-independent) model. Significant test results were often obtained with sloppy data, with data that clearly violate the basic assumptions of the test and with other data where an interpretation of the results in terms of densitydependent regulation was absurd. Given the fact that other explanations have to be found for significant test results for all these cases, mechanisms other than regulation may very well be applicable too where the data are entirely appropriate for the test. The test is simply a data-based choice between a model without and one with a stochastic equilibrium. A time series as such does not contain any information about the causes of the fluctuation pattern, so that one cannot expect statistics to produce such information from that time series. A significant test result using suitable data is entirely consistent with the hypothesis of density-dependent regulation, but also with any other suitable hypotheses. Because the test results were generally consistent with the hypothesis of a universal applicability of the density-dependence model, a negative test result may only mean that the time series was not long enough for the density dependence that was present to become statistically significant. Positive results are difficult to interpret, but so are negative results. A final decision needs to be based not so much on the test result as on much detailed information about the population concerned. Because the density-dependence test does not test for the presence of the mechanism of density-dependent regulation and because of the loaded, multiple meanings of the term density-dependence, calling the test a test of statistical density dependence may be preferable.     

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.

     

Age-dependent changes in plasma biochemistry of yellow-legged gulls (Larus cachinnans)

The study of avian plasma chemistry is providing useful reference values for the management of endangered and game species, supporting veterinarians in their diagnostics, and also bringing to light relevant physiological adaptations during periods of food-shortage. Age is an important source of variability for plasma chemistry. Here I report plasma chemistry of yellow-legged gulls Larus cachinnans from different ages, between post-independence and adulthood, a 5-year interval. Increase in plasma cholesterol concentration and decreases in uric acid, inorganic phosphorus and alkaline phosphatase values were seen. Body mass corrected by body size (i.e. body condition) increased with age, plasma cholesterol being positively correlated in females, but not in males. Moreover, cholesterol was also positively correlated to gonad size in both sexes. Long-term developmental changes in this species, such as gonad development and the acquisition of an optimal body mass for reproduction, could explain these findings. Finally, inorganic phosphorus and alkaline phosphatase, both traditionally related to osteogenesis, were not associated to deferred skull ossification, as originally was suggested in other species.     

Glutamine metabolism in uricotelic species: variation in skeletal muscle glutamine synthetase, glutaminase, glutamine levels and rates of protein synthesis

High intracellular glutamine levels have been implicated in promoting net protein synthesis and accretion in mammalian skeletal muscle. Little is known regarding glutamine metabolism in uricotelic species but chicken breast muscle exhibits high rates of protein accretion and would be predicted to maintain high glutamine levels. However, chicken breast muscle expresses high glutaminase activity and here we report that chicken breast muscle also expresses low glutamine synthetase activity (0.07±0.01 U/g) when compared to leg muscle (0.50±0.04 U/g). Free glutamine levels were 1.38±0.09 and 9.69±0.12 nmol/mg wet weight in breast and leg muscles of fed chickens, respectively. Glutamine levels were also lower in dove breast muscle (4.82±0.35 nmol/mg wet weight) when compared to leg muscle (16.2±1.0 nmol/mg wet weight) and much lower (1.80±0.46 nmol/mg wet weight) in lizard leg muscle. In fed chickens, rates of fractional protein synthesis were higher in leg than in breast muscle, and starvation (48 h) resulted in a decrease in both glutamine content and rate of protein synthesis in leg muscle. Thus, although tissue-specific glutamine metabolism in uricotelic species differs markedly from that in ureotelic animals, differences in rates of skeletal muscle protein synthesis are associated with corresponding differences in intramuscular glutamine content.     

Presence and Abundance of Birds in an Atlantic Forest Reserve and Adjacent Plantation of Shade-Grown Yerba Mate,in Paraguay

In the Atlantic forest region, there is a need to develop economic activities that can be carried out in buffer zones around parks, with minimal impact on forest bird species. One such possibility is the farming of yerba mate, Ilex paraguariensis, under native trees. We compared bird speciesȁ9 presence and abundance between a forest reserve and an adjacent plantation of shade-grown yerba mate, to determine which species might use such plantations. Of the 145 species that were regularly recorded in the forest, 66%, including five globally threatened species, were also regularly recorded in the plantation. Most canopy species and tree trunk insectivores showed similar abundance in both habitats, but forest floor and understory species were absent from the plantation. Within the plantation, higher tree density did not lead to a greater abundance of forest birds. Yerba mate grown under native trees could be used to rehabilitate cleared land and allow recolonization by some Atlantic forest bird species.     

Fruit characteristics and factors affecting fruit removal in a Panamanian community of strangler figs

We describe fruiting characteristics for 12 species in a community of strangler figs (Moraceae: Urostigma) studied in Panama. We quantify diurnal and nocturnal removal rates and proportions of fruits removed, and relate them to the activities of the main dispersers of the figs: bats and birds. These results combined with previous studies show that there are clear differences between fig species with fruit that ripen red and those with fruit that remain green(ish). In the red-fruited species, the fruit are small, ripen asynchronously over relatively long periods, produce little scent, and are mainly taken during the day by birds. In contrast, in the green(ish)-fruited species, the fruits are larger, span a range of sizes, ripen relatively synchronously, produce very distinctive aromas, and are mainly taken at night by bats. This dichotomy in fruiting characteristics suggests coadaptive links between groups of dispersers and different species within the genus Ficus. All fig species produce a range of fruit crop sizes (10–155 fuits/m² canopy area) of which a high proportion were removed by seed dispersers (>80%). Removal rates (fruit removed per day) were positively correlated with crop size, suggesting that trees with large crop size attract more frugivores. Removal rates of green-fruited figs were significantly lower and persistence and abortion of ripe fruit were significant higher around full moon, apparently due to the reduced activity of bats. We further estimate the number of bats that are sustained by a tree fruit crop and account for the observed fruit removal. We then discuss the evidence for coadaptation between different groups of figs and their seed dispersers, Finally, we consider the conservation implications for figs as keystone resources in tropical forests. Received: 26 April 1999 / Accepted: 10 January 2000