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Abstract

Cenozoic reptiles are characterized by physiological morphological and ecological systems with low energy requirements compared to those of mammals. Ectothermy and low resting rates of metabolism are the primary physiological adaptations of reptiles that produce low energy demand. Adjustments of the oxygen-transport system to different thermoregulatory characteristics among reptiles may be reflected in blood viscosity oxygen capacity oxygen affinity and the temperature sensitivity of oxygenation. Other adaptations reduce the energy cost of oxygen transport. Reptiles have low hematocrits and large, widely spaced capillaries that contribute to a low fluid resistance in the vascular system but also limit the oxygen transport capacity. The low oxygen affinity characteristic of the blood of most reptiles appears to facilitate diffusion of oxygen to the tissues, overcoming the intrinsic limitations imposed by the morphological specializations of the cardiovascular system. The low blood oxygen affinity permits virtually all of the oxygen carried by the blood to be delivered to the tissues during periods of stress. It may also help to maintain a relatively high arterial Po 2 even when a right-to-left shunt occurs in the heart. Reptilian erythrocytes are capable of reducing methemoglobin rapidly. The high concentrations of methemoglobin and polymerized hemoglobin that occur in vivo may indicate that these compounds have a functional role. In their blood physiology as in other aspects of their biology reptiles are specialized animals that reflect selective forces quite different from those that have shaped the evolution of mammals.
... The cumulative genetic modifications that facilitated the development of endothermic animals coded for structural changes that enhanced the delivery of O 2 to the lungs for gas exchange (Lovegrove, 2017) and greatly increased the density of capillary beds in muscle/tissues for CO 2 /O 2 gas exchange (Pough, 1980a). ...
... The average capillary surface area per unit volume of tissue is about six times greater in mammals than reptiles. The average diffusion distance between the reptilian capillary and cell is about 2.5 times that in the mammalian system (Pough, 1980a;Schulte et al., 2015). The reptilian hematocrit is also quite low with an average of 28% and an O 2 capacity of 8.7 ml/100 ml blood for 83+ species tested (Pough, 1980a). ...
... The average diffusion distance between the reptilian capillary and cell is about 2.5 times that in the mammalian system (Pough, 1980a;Schulte et al., 2015). The reptilian hematocrit is also quite low with an average of 28% and an O 2 capacity of 8.7 ml/100 ml blood for 83+ species tested (Pough, 1980a). As we will discuss below many of these metric parameters may greatly affect thrombocyte/platelet reactions in hemostasis and exchange of gases by RBCs. ...
Article
This review presents evidence to support the hypothesis that the reduced O2 during the Permian/Triassic period was the impetus for the evolutionary selection of endothermic animals. The evolution of smaller red blood cells with greater surface areas along with increased: capillary density, capillary surface area, hematocrits, blood pressure, blood flow rates, and shear rates were critical for efficient gas exchange in endothermy. The evolution of the four-chambered mammalian/avian heart allowed for low pulmonary and high systemic blood pressure. It is proposed that hypoxia-induced angiogenesis led to increased vascularization in endothermic animals. The increased blood pressure, flow rates, and shear forces likely required changes in hemostatic mechanisms that were met in mammals by the evolution of anucleate platelets. The evolution of mammals and birds occurred in a parallel fashion with further genetic changes to anucleate RBCs/platelets occurring in mammals. Although it is possible that the evolution of endothermy in birds and mammals occurred as two independent events, it is more likely that a common ancestor developed genetic mutations that laid down the road map for parallel alterations of their cardiovascular system in response to environmental pressures. Model systems to support the proposed changes from ectotherm to endotherm were developed from published data. The evolutionary development of endothermy occurred over millions of years with a continuum of genetic alterations that involved skeletal, soft tissue, cardiovascular macrochanges along with numerous molecular alterations. Genetic signals and potential regulators for the evolutionary changes of endothermic blood cells from their bipotential stem cells are also proposed.
... Recent findings in zebra finches suggest that birds-despite being endotherms-reduce their hematocrit, number of erythrocytes, and content of hemoglobin when acclimated to cold temperatures below the thermoneutral zone (Niedojadlo et al. 2018). Such response may be explained as an optimization in blood viscosity alleviating physical constraints to blood flow imposed by poor deformability of erythrocytes due to their nucleation (Niedojadlo et al. 2018;Pough 1980). Even more counterintuitive patterns seem to occur in non-avian reptiles where an increase in hematological variables was observed in response to cold acclimation, despite the well-known effect of lowered metabolism at low temperatures (MacMahon and Hamer 1975). ...
... Accordingly, we predict that erythrocytes will shrink at higher temperature. Such a phenotypic flexibility could be linked to the possible effect of lowering blood viscosity (Pough 1980;Snyder and Sears 2006) and high surface-tovolume ratio of smaller cells, which may have a positive effect oxygen uptake and release (Yamaguchi et al. 1987;Kozlowski et al. 2003;Gregory 2002;Starostová et al. 2009). Therefore, smaller cell size at high temperature would compensate for the anticipated lower cell number. ...
... Hematological variables affect oxygen supply not only by defining the oxygen-carrying capacity, but they are also tightly coupled to the efficiency of oxygen transport through blood circulation in vessels. More specifically, the more erythrocytes are in the blood, the thicker and more viscous the blood is (Pough 1980;Windberger and Baskurt 2007). In turn, high viscosity of blood increases shear stress and vessel resistance, which sets constraints to the blood flow and increases the workload of the whole cardiovascular system (Guyton and Richardson 1961;Fowler and Holmes 1975). ...
Article
Acclimation to lower temperatures decreases energy expenditure in ectotherms but increases oxygen consumption in most endotherms, when dropped below thermoneutrality. Such differences should be met by adjustments in oxygen transport through blood. Changes in hematological variables in correspondence to that in metabolic rates are, however, not fully understood, particularly in non-avian reptiles. We investigated the effect of thermal acclimation on a snake model, the grass snakes (Natrix natrix). After 6 months of acclimation to either 18 °C or 32 °C hematocrit, hemoglobin concentration, erythrocyte number, and size were assessed. All variables revealed significantly lower values under warm compared to cold ambient temperature. Our data suggest that non-avian reptiles, similarly as birds, reduce erythrocyte fraction under energy-demanding temperatures. Due to low deformability of nucleated erythrocytes in sauropsids, such reduced fraction may be important in decreasing blood viscosity to optimize blood flow. Novel findings on flexible erythrocyte size provide an important contribution to this optimization process.
... Both the Hct/PCV and hemoglobin of mallards ( (Pough, 1980); and Testudines: 7.97 g dL −1 ; Dessauer, 1970, 8.5 g dL −1 ; Pough, 1980]. The last common ancestor being the following: ...
... Both the Hct/PCV and hemoglobin of mallards ( (Pough, 1980); and Testudines: 7.97 g dL −1 ; Dessauer, 1970, 8.5 g dL −1 ; Pough, 1980]. The last common ancestor being the following: ...
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Physiologically based kinetic (PBK) models are a promising tool for xenobiotic environmental risk assessment that could reduce animal testing by predicting in vivo exposure. PBK models for birds could further our understanding of species-specific sensitivities to xenobiotics, but would require species-specific parameterization. To this end, we summarize multiple major morphometric and physiological characteristics in chickens, particularly laying hens (Gallus gallus) and mallards (Anas platyrhynchos) in a meta-analysis of published data. Where such data did not exist, data are substituted from domesticated ducks (Anas platyrhynchos) and, in their absence, from chickens. The distribution of water between intracellular, extracellular, and plasma is similar in laying hens and mallards. Similarly, the lengths of the components of the small intestine (duodenum, jejunum, and ileum) are similar in chickens and mallards. Moreover, not only are the gastrointestinal absorptive areas similar in mallard and chickens but also they are similar to those in mammals when expressed on a log basis and compared to log body weight. In contrast, the following are much lower in laying hens than mallards: cardiac output (CO), hematocrit (Hct), and blood hemoglobin. There are shifts in ovary weight (increased), oviduct weight (increased), and plasma/serum concentrations of vitellogenin and triglyceride between laying hens and sexually immature females. In contrast, reproductive state does not affect the relative weights of the liver, kidneys, spleen, and gizzard.
... This difference in oxygen affinity between maternal and fetal blood is common among reptiles (Blackburn, 2000b;Pough, 1980) and is present in most vertebrates where these values have been measured (Ingermann, 1992). Gravid viviparous snakes can reduce maternal hemoglobin oxygen affinity below that of embryos so that embryos have a relatively higher oxygen affinity (Holland et al., 1990;Ingermann, 1992). ...
... affinity of hemoglobin decreases with increasing temperature (Dessauer, 1970;Hill et al., 2004;Pough, 1980). Hence, some of the lowest oxygen environments on earth are at high elevations in lower (and warmer) latitudes, which are precisely the areas with the highest relative frequencies of viviparous species within reproductively bimodal genera (Guillette et al., 1980;Hodges, 2004;Lambert & Wiens, 2013;Watson et al., 2014). ...
Article
Research focused on understanding the evolutionary factors that shape parity mode evolution among vertebrates have long focused on squamate reptiles (snakes and lizards), which contain all but one of the evolutionary transitions from oviparity to viviparity among extant amniotes. While most hypotheses have focused on the role of cool temperatures in favoring viviparity in thermoregulating snakes and lizards, there is a growing appreciation in the biogeographic literature for the importance of lower oxygen concentrations at high elevations for the evolution of parity mode. However, the physiological mechanisms underlying how hypoxia might reduce fitness, and how viviparity can alleviate this fitness decrement, has not been systematically evaluated. We qualitatively evaluated previous research on reproductive and developmental physiology, and found that (1) hypoxia can negatively affect fitness of squamate embryos, (2) oxygen availability in the circulatory system of adult lizards can be similar or greater than an egg, and (3) gravid females can possess adaptive phenotypic plasticity in response to hypoxia. These findings suggest that the impact of hypoxia on the development and physiology of oviparous and viviparous squamates would be a fruitful area of research for understanding the evolution of viviparity. To that end, we propose an integrative research program for studying hypoxia and the evolution of viviparity in squamates.
... 26.433090 doi: bioRxiv preprint affinities between major classes of vertebrates (e.g. mammals versus reptiles), 18,19 any significant inter-class differences in myoglobin net charge and surface hydrophobicity remain to be identified. 20 In this study, we modeled the tertiary structures of 302 vertebrate myoglobin orthologs and found significant differences in net charge and surface hydrophobicity between major classes of vertebrates. ...
... Perhaps the lower myoglobin net charge of reptiles is a byproduct, or even a cause for, the lower oxygen affinities of reptilian globins compared to those of mammals. 18,19 Due to the abundance of mammalian myoglobin orthologs, differences in net charge between major mammalian orders were also investigated, excluding aquatic species. The results showed that myoglobin net charge for different mammalian orders is quite similar, although the myoglobin . ...
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Myoglobin is the major oxygen carrying protein in vertebrate muscle. Previous studies identified in secondarily aquatic mammalian lineages high myoglobin net charge, which serves to prevent aggregation at the extremely high intracellular myoglobin concentrations found in these species. However, it is unknown how aquatic birds that dive for extended durations prevent myoglobin aggregation at their high intracellular myoglobin concentrations. It is also unknown whether secondarily aquatic lineages reduced the surface hydrophobicity of their myoglobins to prevent aggregation. Here, we used a deep learning-predicted distance-based protein folding algorithm to model the tertiary structures of 302 vertebrate myoglobin orthologs and performed a comparative analysis of their predicted net charge and surface hydrophobicities. The results suggest that aquatic avian divers, such as penguins and diving ducks, evolved highly charged myoglobins to reduce aggregation propensity and allow greater storage of oxygen for extended underwater foraging. High myoglobin net charge was also identified in golden eagles, a species that routinely suffers high-altitude hypoxia. Although no general association was found between myoglobin surface hydrophobicity and intracellular concentration, comparison of predicted net charge and surface hydrophobicities revealed significant differences between major vertebrate classes; bird myoglobins are the most positively charge, reptile myoglobins are the most negatively charged, and the myoglobins of ray-finned fish (Actinopterygii) have higher surface hydrophobicity than those of lobe-finned fish (Sarcopterygii). Our findings indicate the convergent evolution of high myoglobin net charge in aquatic birds and mammals, and offer novel insights into the diversification of myoglobin among vertebrate clades.
... Whether snakes have lower threshold to MetHb toxicity than mammals is unknown as threshold data for reptiles are unavailable. In comparison to mammals and birds, reptiles generally have lower hematocrits and lower erythrocyte counts, lower hemoglobin contents, lower blood oxygen capacities, and lower capillary densities 11 , all of which result in comparatively low delivery rates of oxygen to tissues. However, blood oxygen affinities of reptiles are lower than those of mammals 11 . ...
... In comparison to mammals and birds, reptiles generally have lower hematocrits and lower erythrocyte counts, lower hemoglobin contents, lower blood oxygen capacities, and lower capillary densities 11 , all of which result in comparatively low delivery rates of oxygen to tissues. However, blood oxygen affinities of reptiles are lower than those of mammals 11 . Studies in fish have demonstrated that the critical thermal maximum (the body temperature at which the righting response is lost) is inversely related to methemoglobin level 12 , but it is unknown whether this relationship holds in reptiles or whether field-operative body temperatures of brown treesnakes place them at a somewhat lower threshold to methemoglobin toxicity than most mammals. ...
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The invasive brown treesnake (Boiga irregularis) has extirpated much of Guam’s native birdlife and poses significant threats to other parts of the western Pacific. Acetaminophen (APAP) is a proven lethal oral toxicant in reptiles but the physiological mechanism is unknown. The effects of a lethal APAP oral dose on methemoglobin (MetHb, non-oxygen carrying form) levels and other blood parameters were examined in brown treesnakes. Co-oximetry was used to measure MetHb (%) and other hemoglobin species. Assessment of red blood cell integrity, white blood cell differential counts, and plasma biochemical analyses were conducted to evaluate tissue damage, stress, and liver function. Changes in oxygen carrying capacity were noted in APAP-treated snakes indicated by a 50–60% increase in methemoglobin levels and a 40% decrease in oxyhemoglobin (oxygen-carrying form) levels compared to controls. APAP-treated snakes had decreased lymphocyte and increased monocyte counts while also having increased levels of blood analytes associate with impaired liver function and muscle damage. The proximate cause of death in APAP-treated snakes was likely acute methemoglobinemia and respiratory failure due to severe hypoxia with no observed signs of distress or pain. An orally-ingested lethal dose of APAP appears to be a humane method for lethal control of this species.
... Oxygen flux in embryonic 857 mammals is largely determined by oxygen-diffusing capacity of the placenta, the rates of blood 858 flow in the umbilical and uterine arteries, and the oxygen capacities and affinities of fetal and 859 maternal blood (Carter, 2009). Reptilian and mammalian blood vessels differ in basic 860 characteristics such as capillary density, capillary surface, and oxygen diffusion gradients 861 (Pough, 1980). 862 ...
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Across amniotes, squamates represent the only clade with highly variable parity modes, oviparity (egg-laying) and viviparity (live-birth). Despite this, relatively little is known about how oviparity and viviparity evolve at the genomic and physiological levels in squamates. Within the context of interdisciplinary medical, poultry science, and reproductive biology literature, I review the genomics and physiology of reproduction across five broad processes expected to change during transitions between parity modes—eggshell formation, embryonic retention, placentation, calcium transport, and maternal-fetal immune dynamics. This review is the first time that the maternal-fetal immune dynamics of squamates is considered in the context of modern medical literature, where embryos are no longer conceptualized as analogs to allografts. I offer alternative perspectives and holistic hypotheses on the genomic and transcriptomic drivers of parity mode transitions in squamates. Two new pathways through which early Lepidosaurs may have transitioned rapidly between oviparity and viviparity with no intermediate stages are presented. Overall, the physiology of reproduction illuminates the biological plausibility of highly labile parity modes in some squamate lineages, with constrained parity modes in others. Future research should be open to either possibility unless clade-specific biological evidence suggests otherwise. Rather than emphasizing the feasibility of transitions in either direction, I posit that oviparity and viviparity are relatively minor variations of a shared process.
... All examined crocodilian species exhibited low hematocrits and Hb concentrations (Table 2), consistent with previous studies (45), and reflecting the low blood-O 2 carrying capacities of reptiles. ...
Chapter
Respiratory anatomy and physiology in reptiles and amphibians are extremely variable among species and starkly different than seen in mammals. This cannot be exemplified more than by the cutaneous respiration ability and lack of lungs in many amphibian species. Methods for providing oxygen therapy must accommodate these differences. Hypoxia can be difficult to determine and oxygen therapy can actually suppress spontaneous respiration in reptiles. This chapter offers an overview of oxygen therapy in reptiles and amphibians, and the methods in which it can be implemented.
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Most of the cerebral microcirculation is comprised of capillaries that are lined with pericytes, but the influence of pericytes on local blood flow was not previously established. A new study by Hartmann and colleagues uses selective optical ablation or activation to demonstrate that capillary pericytes exert both static and slow types of regulation on capillary diameter to affect flow, which are distinct from canonical rapid regulation by arteriole smooth muscle.
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1.1. Oxygen affinity of blood of five lizard species was measured at 25, 35 and 40°C and pCO2's of 38 and 76 mm Hg.2.2. At its activity temperature each species had a P50 of 68–72 mm Hg. Oxygen affinity was also related to body size.3.3. There was a seasonal shift in oxygen affinity in Dipsosaurus dorsalis.4.4. There was no difference in oxygen affinity of blood of Sceloporus occidentalis from sea level and from 6000 ft.5.5. There was no correlation between sensitivity to CO2 and fossorial habits.6.6. An anguid (Gerrhonotus multicarinatus) showed less sensitivity to changes in temperature and pCO2 than iguanids.
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Blood oxygen affinity of 15 species of colubrine snakes is related to body size by the equation . Blood oxygen affinity of snakes in six other families did not differ from values predicted for colubrines of the same body size. An ontogenetic decrease in blood oxygen affinity was found in three of four species for which adequate samples were available. This ontogenetic change was seen only in whole blood; there was no ontogenetic change in oxygen affinity of hemoglobin in solution. The decrease in blood oxygen affinity with increasing body size (ontogenetic growth or adult body size) in snakes contrasts with the increase in oxygen affinity with increasing body size in mammals, birds, and lizards. The difference in blood oxygen affinity probably reflects the differences in pulmonary gas concentrations produced by specialized lung morphology and breathing movements of snakes.
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Oxygen capacity of reptile blood in vitro is temperature sensitive and is reversibly reduced as much as 40% at the extremes of the temperature range that animals normally encounter. In several species of lizards and snakes, blood oxygen capacity is maximum within the species' activity-temperature range. The correlation coefficient between eccritic temperature and the temperature giving maximum blood oxygen capacity for all species tested was .79 (P < .01). (When the genera Sceloporus and Uta, which show a different pattern, are omitted from the analysis, the correlation coefficient for the remaining species rises to .92.) This adaptation of the blood is one of the mechanisms that produces maximum oxygen consumption near a species' eccritic temperature. In lizards of the genera Sceloporus and Uta and in turtles the maximum blood oxygen capacity occurs at the bottom of the activity-temperature range and may reflect adaptation of these animals to activity at low temperatures.
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Hemoglobin content was significantly different in blood of Sceloporus jarrovi collected at altitudes of 5,500, 8,300, and 8,600 ft. These differences were correlated with environmental temperature regimes, with hemoglobin content being greater in cooler habitats. Hemoglobin content was significantly higher in winter (February) than in summer (July) at both 5,500 and 8,300 ft. Slight changes in hemoglobin after acclimation to 4,900 ft for 2 mth were attributed to temperature differences rather than other altitude related differences. Hemoglobin values higher than those previously reported were probably a result of the unusually cold winter of 1973.
1.1. Red blood cells were analyzed for ATP, 2,3-diphosphoglycerate and inositol polyphosphate at different stages of development of two birds; pigeon and Western gull, and several reptiles: Pacific Ridley, snapping and Pseudemys turtles; green iguana, yellow rat snake and American alligator. Other species were examined only as juveniles or adults: ostrich, Boa constrictor and the Nile and Moreleti crocodiles. The results were compared with the phosphate compounds found in red cells of adult man, rat and rabbit.2.2. The presence, concentration, and time of occurrence of diphosphoglycerate and inositol polyphosphate, separately or together, during development, provided new biochemical clues to evolutionary relationships.3.3. Remarkably large differences in the concentration of ATP in red cells during the development of an animal, and among different kinds of animals, could not be explained.
1.1. Oxygen affinity of whole blood of 51 species of lizards from 12 families was measured at the eccritic temperature of each species.2.2. Blood oxygen affinity was lower than that of birds or mammals and increased with increasing body size.3.3. Iguanid lizards were used as a basis for comparisons of other families. Blood oxygen affinity of lizards in the families Agamidae, Cordylidae, Lacertidae and Varanidae did not differ from that of iguanids of comparable body size.4.4. Teiid and anguid lizards had lower oxygen affinities than iguanids. possibly reflecting their more active lives.5.5. Scincid and chamaeleonid lizards had higher blood oxygen affinities than iguanids, apparently as a result of their lower eccritic temperatures.6.6. Geckonid and xantusiid lizards had higher blood oxygen affinities than iguanids at their normally low eccritic temperatures and at higher temperatures comparable to eccritic temperatures of iguanid lizards.