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A) overview illustrating mucosa with alveolar mucous glands. Note interstitial connective tissue (lamina propria) between the glands contains many blood vessel profiles. The deep vascular layer lies between the tracheal cartilage and the mucosa. B) detail of an alveolar mucous gland showing goblet cells (only one indicated) at its entrance. Note the proximity of the most superficial blood vessels to the luminal surface of the ciliated epithelium. Scale indicated by bars. Staining of 2 µm thick sections with 0.1% toluidine blue.
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Various parts of the respiratory system play an important role in temperature control in birds. We create a simplified computational fluid dynamics (CFD) model of heat exchange in the trachea and air sacs of the domestic fowl (Gallus domesticus) in order to investigate the boundary conditions for the convective and evaporative cooling in these part...
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The origin of the air sac system present in birds has been an enigma for decades. Skeletal pneumaticity related to an air sac system is present in both derived non-avian dinosaurs and pterosaurs. But the question remained open whether this was a shared trait present in the common avemetatarsalian ancestor. We analyzed three taxa from the Late Trias...
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... The peculiar anatomic characteristics of the respiratory apparatus of birds make them particularly susceptible to aspergillosis: absence of epiglottis and diaphragm, limited distribution of pseudostratified ciliated columnar cells at the epithelium surface [16], presence of air sacs where elevated moisture and local temperature (40-43.5°C in average) can favor fungal growth and facilitate proximal dissemination to lungs [36]. Aspergillosis is a devastating fungal disease for penguins that live in captivity under managed care [3][4][5]10,13,16,37], whereas its overall incidence is assumed to remain very low into the wild [38]. ...
Aspergillosis is pervasive in bird populations, especially those under human care. Its management can be critically impacted by exposure to high levels of conidia and by resistance to azole drugs.
The fungal contamination in the environment of a Humboldt penguin (Spheniscus humboldti) group, housed in a French zoological park next to numerous large crop fields, was assessed through three serial sessions of surface sampling in nests, in 2018-20: all isolates were counted and characterized by sequencing. When identified as A. fumigatus, they were systematically screened for resistance mutations in the cyp51A gene and tested for MICs determination. In the same time, the clinical incidence of aspergillosis was evaluated in the penguin population by the means of systematic necropsy and mycological investigations. A microsatellite-based analysis tracked the circulation of A. fumigatus strains.
Environmental investigations highlighted substantial increase of the fungal load during the summer season (>12-fold vs. the other timepoints) and large overrepresentation of species belonging to the Aspergillus section Fumigati, ranging from 22.7 to 94.6% relative prevalence. Only one cryptic species was detected (A. nishimurae), and one isolate exhibited G138S resistance mutation with elevated MICs. The overall incidence of aspergillosis was measured at ∼3.4% case-years, and mostly in juveniles. The analysis of microsatellite polymorphism revealed a high level of genetic diversity among A. fumigatus clinical isolates. In contrast, one environmental strain appeared largely overrepresented during the summer sampling session. In all, the rural location of the zoo did not influence the emergence of resistant strains.
... Because only cervical and abdominal air sacs and lungs can produce pneumatic diverticula that invade the vertebrae (O'connor and Claessens 2005), the presence of a sophisticated pneumatic complex along the neck of lessemsaurids (and in dorsal series of other non-gravisaurian sauropodiforms) suggests that a cervical air sac system was already well-developed among early-diverging Sauropodiformes during Norian times, 20 myr before the gravisaurians. This improved avianstyle respiratory system observed among non-gravisaurian sauropodiforms (mainly in lessemsaurids) may also be related to the need to lose heat, especially if their extremely high bone growth rate necessitated a high metabolic rate (Sverdlova et al. 2012;Henderson 2013;Sander 2013b;. Cyclical and remarkably high bone growth rates represent a key lessemsaurids novelty which helped them attain large body sizes through a strategy of accelerated growth distinct from that associated with gigantism in eusauropods ). ...
After the extinction of rebbachisaurids during the Cenomanian–Turonian interval, titanosaurs were the only group of sauropods to face the K–Pg event. This same global pattern also holds for the end-Cretaceous (Campanian–Maastrichtian) titanosaur record in South America, where their remains can be found from southern Argentina to Ecuador, with more frequent findings in Argentina and Brazil. In this chapter, we review these fossil findings and the main aspects of the taxonomy, systematics, and paleogeographic implications of this record and briefly discuss the importance of these occurrences for the understanding of titanosaur evolution. The diversity and abundance of end-Cretaceous titanosaur taxa in South America represent about 25% of the known Titanosauria species in the world, which makes them the most common group of large terrestrial herbivores of that time. Cretaceous titanosaurs from South America also vary highly in morphology and size, comprising small to large-sized taxa, for example. Their record mainly consists of appendicular and axial remains, including rare skull material, but also comprises eggs, nests, footprints, and coprolites. In South America, by the end of the Late Cretaceous, titanosaurs were generally represented by more derived titanosaurians that are mainly taxonomically assigned to more derived species within Aeolosaurini and Saltasaurinae.
... Thus, latent losses were not actually modeled and core body temperature was not included in the model. However, the respiratory system plays an important role in controlling the body temperature of birds, being essential in the heat balance (Sverdlova et al., 2012;Silva and Maia, 2012;Nascimento et al., 2017). Furthermore, in the study developed by Tickle and Codd (2019), the influence of air velocity was not evaluated experimentally, making better analysis of sensitive exchanges impossible. ...
... Respiration rate is directly related to the classification of the thermal comfort status of animals (Kassim and Sykes, 1982;Sverdlova et al., 2012), preceding the changes in the t clo (Yahav et al., 2005;Santana et al., 2017). It was observed that only the t air factor was significant (p < 0.05) when the ANOVA was performed for RR. ...
... The latent exchanges (Q Resp ) demand a higher metabolic cost than sensible exchanges (Yahav et al., 2004;Ruzal et al., 2011;Sverdlova et al., 2012). Simmons et al. (1997) , when exposing broilers to V air of 1.0, 1.5, 2.0, 2.5, and 3.0 m⋅s − 1 , observed a reduction in latent heat for all used t air (29, 32, and 35 • C) when V air increased. ...
The objective of this study was to develop a heat balance in laying hens and analyze their performance, besides simulating the partition between sensible and latent heats. The 28-d old Hy-line laying hens were subjected to a factorial combination of five levels of air temperature (20, 24, 28, 32, and 36 • C), two levels of air relative humidity (40 and 60%), and three levels of air velocity (0.2, 0.7 and 1.4 m•s − 1). The minimum and maximum exposure times for each bird to a given thermal challenge were 3 h and 6 h, respectively. Firstly, ANOVA and multiple regression were performed to fit equations of respiratory rate and the overall heat transfer coefficient by conduction in the bird's body (U), respectively. For the heat balance, the partitions of heat transferred to the bird's body through conduction, convection, radiation and respiratory tract were taken into account. Different input settings were evaluated for convection heat transfer coefficient (h conv) and U. The validation of the proposed model was performed by comparing the predicted cloacal temperature values to those obtained experimentally. As a result, the model proved to be adequate for analyzing the interaction between hen and environment, and the complexity in determining U and h conv interferes in its performance. Statistical analysis reiterates that the use of constant values for these coefficients are not recommended. For the studied conditions, latent heat loss had a greater contribution than sensible forms from the temperature of 32.85 • C, not being influenced by air velocity. The model is accurate for the prediction of cloacal temperature, contributing to the identification of possible strategies for mitigating thermal stress, as it allows simulations of the thermoregulation mechanism of laying hens.
... Gigantism in eusauropods has been proposed as the result of a complex interplay of anatomical, physiological and reproductive intrinsic traits [12][13][14][15][16][17][18][19][20] . In this context, their elongated neck was interpreted as a key acquisition that-among others-improved heat loss allowed by the avian-like cervical air sacs and the neck's high surfaceto-volume ratio, as required given the high metabolic rate inferred for eusauropods 15,40,41 . The pneumatic structures present in the cervical vertebrae of Ingentia and Lessemsaurus, and in the dorsal vertebrae of Antetonitrus 27,31 , suggest the presence of an avian-like respiratory system in lessemsaurids that was more developed in terms of invading the axial skeleton than in basal sauropodomorphs. ...
Dinosaurs dominated the terrestrial ecosystems for more than 140 Myr during the Mesozoic era, and among them were sauropodomorphs, the largest land animals recorded in the history of life. Early sauropodomorphs were small bipeds, and it was long believed that acquisition of giant body size in this clade (over 10 tonnes) occurred during the Jurassic and was linked to numerous skeletal modifications present in Eusauropoda. Although the origin of gigantism in sauropodomorphs was a pivotal stage in the history of dinosaurs, an incomplete fossil record obscures details of this crucial evolutionary change. Here, we describe a new sauropodomorph from the Late Triassic of Argentina nested within a clade of other non-eusauropods from southwest Pangaea. Members of this clade attained large body size while maintaining a plesiomorphic cyclical growth pattern, displaying many features of the body plan of basal sauropodomorphs and lacking most anatomical traits previously regarded as adaptations to gigantism. This novel strategy highlights a highly accelerated growth rate, an improved avian-style respiratory system, and modifications of the vertebral epaxial musculature and hindlimbs as critical to the evolution of gigantism. This reveals that the first pulse towards gigantism in dinosaurs occurred over 30 Myr before the appearance of the first eusauropods.
... A long neck also plays a role in heat loss through an avian-style respiratory system, as discussed below [166]. The long neck was thus part of a positive feedback loop, in which it supported the high BMR of sauropods through its role in thermoregulation (Fig. 8). ...
... The respiratory system of extant birds is well known to function in body temperature control, raising the question whether this function was served by the ARS hypothesized for sauropods [140,141]. A novel modeling approach, computational fluid dynamics (CFD), can be used to assess the function of the ARS in heat loss [166]. A two-dimensional CFD model of heat exchange in the trachea and air sacs of domestic chicken was used to validate the method [166]. ...
... A novel modeling approach, computational fluid dynamics (CFD), can be used to assess the function of the ARS in heat loss [166]. A two-dimensional CFD model of heat exchange in the trachea and air sacs of domestic chicken was used to validate the method [166]. A three-dimensional CFD simulation of the respiratory tract of a sauropod would serve to test the hypothesis. ...
Sauropod dinosaurs are a group of herbivorous dinosaurs which exceeded all other terrestrial vertebrates in mean and maximal body size. Sauropod dinosaurs were also the most successful and long-lived herbivorous tetrapod clade, but no abiological factors such as global environmental parameters conducive to their gigantism can be identified. These facts justify major efforts by evolutionary biologists and paleontologists to understand sauropods as living animals and to explain their evolutionary success and uniquely gigantic body size. Contributions to this research program have come from many fields and can be synthesized into a biological evolutionary cascade model of sauropod dinosaur gigantism (sauropod gigantism ECM). This review focuses on the sauropod gigantism ECM, providing an updated version based on the contributions to the PLoS ONE sauropod gigantism collection and on other very recent published evidence. The model consist of five separate evolutionary cascades ("Reproduction", "Feeding", "Head and neck", "Avian-style lung", and "Metabolism"). Each cascade starts with observed or inferred basal traits that either may be plesiomorphic or derived at the level of Sauropoda. Each trait confers hypothetical selective advantages which permit the evolution of the next trait. Feedback loops in the ECM consist of selective advantages originating from traits higher in the cascades but affecting lower traits. All cascades end in the trait "Very high body mass". Each cascade is linked to at least one other cascade. Important plesiomorphic traits of sauropod dinosaurs that entered the model were ovipary as well as no mastication of food. Important evolutionary innovations (derived traits) were an avian-style respiratory system and an elevated basal metabolic rate. Comparison with other tetrapod lineages identifies factors limiting body size.
Birds have high metabolic rates and so require an efficient means of delivering oxygen to their cells and eliminating carbon dioxide, and the avian respiratory system is exceptionally efficient. In this chapter, I describe in detail the anatomy of the avian respiratory system, from the nostrils and oral cavity, past the pharynx and larynx, trachea, and bronchi and to the lungs and air sacs. The process of ventilation, the mechanism by which air moves into, through, and out of the respiratory system, is described. The metabolic cost of breathing and how breathing is altered when birds walk, run, and fly are explained. The role of air sacs in the unidirectional flow of air through the lungs is described, as are other features of the avian lungs that make the exchange of gases between blood and air capillaries so efficient. Finally, the process by which the avian nervous system controls respiration is explained.
The objective of this research was to evaluate the thermal exchanges, physiological responses, productive performance and carcass yield of Guinea Fowl confined under thermoneutral conditions and under thermal stress. For the experiment, 96 animals were confined in 8 experimental boxes of 1 m2 of area, each, divided in equal numbers and placed inside two distinct climatic chambers, where the birds were distributed in a completely randomized design, with two treatments (air temperatures of 26 and 32 °C, respectively). For the collection of physiological responses and carcass yield 16 birds were evaluated and for the collection of data on feed and water consumption and productive responses, 48 birds per treatment were evaluated. The environmental variables (air temperature (AT), air relative humidity and wind speed), temperature and humidity index (THI), heat exchanges, physiological responses (respiratory rate, surface temperature, cloacal temperature and eyeball temperature), feed (FC) and water (WC) consumption and production responses (weight gain, feed conversion index and carcass yield) of the birds were evaluated. With the elevation of the AT, it could be noticed that the THI went from a thermal comfort condition to an emergency condition, where the birds lost part of their feathers, increased all physiological responses evaluated, and consequently, reduced by 53.5% the amount of heat dissipated in the sensible form and increased by 82.7% the heat losses in the latent form, increasing also the WC. ATs of up to 32 °C did not significantly affect the productive performance and carcass yield of the guinea fowl.
Sauropodomorpha was an herbivorous clade of dinosaurs that lived through nearly the entire Mesozoic Era. Sauropodomorphs appeared at the end of the Triassic as small and gracile forms and evolved into the largest land animals that ever lived on Earth. This evolutionary path towards giant forms implied several skeletal modifications and anatomical innovations already recorded at the end of the Triassic that continued to develop throughout the rest of the Mesozoic. Recent discoveries of early-diverging Sauropodiformes from Gondwana shed light on this crucial stage in the history of the group, providing new information about the origin of gigantism among Sauropodomorpha. Non-gravisaurian sauropodiform is the grade of dinosaurs that—despite not being characterized by typical derived or ‘sauropod-like’ features, often regarded as a prerequisite for gigantism (long neck, columnar-limbed, obligated quadrupedal posture)—show the first clear steps towards gigantism. This group is known by moderately gracile to robust forms that attained large body size during the Late Triassic and Early Jurassic. The South American record is restricted to Argentina, including two early-branching forms from Patagonia (Mussaurus patagonicus and Leonerasaurus taquetrensis) and the lessemsaurids Lessemsaurus sauropoides and Ingentia prima, from the north-western region of that country. Here we provide a comprehensive review of these four taxa, highlighting the main plesiomorphic and derived traits that relate them to both early-diverging (Massopoda) and late-diverging (Gravisauria) sauropodomorphs, positioning them as the first steps towards gigantism on Earth.
Air sacs are an important component of the avian respiratory system, and corresponding structures also were crucial for the evolution of sauropod dinosaur gigantism. Inferring the presence of air sacs in fossils so far is restricted to bones preserving internal pneumatic cavities and foramina as osteological correlates. We here present bone histological correlates for air sacs as a new potential identification tool for these elements of the respiratory system. The analysis of several avian and non-avian dinosaur samples revealed delicate fibres in secondary trabecular and secondary endosteal bone that in the former case (birds) is known or in the latter (non-avian dinosaurs) assumed to have been in contact with air sacs, respectively. The bone histology of this 'pneumosteal tissue' is markedly different from those regions where muscles attached presenting classical Sharpey's fibres. The pneumatized bones of several non-dinosaurian taxa do not exhibit the characteristics of this 'pneumosteum'. Our new histology-based approach thus can be instrumental in reconstructing the origin of air sacs among dinosaurs and hence for our understanding of this remarkable evolutionary novelty of the respiratory system.
Increased organismic complexity in metazoans was achieved via the specialization of certain parts of the body involved in different faculties (structure-function complexes). One of the most basic metabolic demands of animals in general is a sufficient supply of all tissues with oxygen. Specialized structures for gas exchange (and transport) consequently evolved many times and in great variety among bilaterians. This review focuses on some of the latest advancements that morphological research has added to our understanding of how the respiratory apparatus of the primarily terrestrial vertebrates (amniotes) works and how it evolved. Two main components of the respiratory apparatus, the lungs as the "exchanger" and the ventilatory apparatus as the "active pump," are the focus of this paper. Specific questions related to the exchanger concern the structure of the lungs of the first amniotes and the efficiency of structurally simple snake lungs in health and disease, as well as secondary functions of the lungs in heat exchange during the evolution of sauropod dinosaurs. With regard to the active pump, I discuss how the unique ventilatory mechanism of turtles evolved and how understanding the avian ventilatory strategy affects animal welfare issues in the poultry industry.
