Maximal aerobic metabolic rates (MMR) in vertebrates are supported by increased conductive and diffusive fluxes of O(2) from the environment to the mitochondria necessitating concomitant increases in CO(2) efflux. A question that has received much attention has been which step, respiratory or cardiovascular, provides the principal rate limitation to gas flux at MMR? Limitation analyses have principally focused on O(2) fluxes, though the excess capacity of the lung for O(2) ventilation and diffusion remains unexplained except as a safety factor. Analyses of MMR normally rely upon allometry and temperature to define these factors, but cannot account for much of the variation and often have narrow phylogenetic breadth. The unique aspect of our comparative approach was to use an interclass meta-analysis to examine cardio-respiratory variables during the increase from resting metabolic rate to MMR among vertebrates from fish to mammals, independent of allometry and phylogeny. Common patterns at MMR indicate universal principles governing O(2) and CO(2) transport in vertebrate cardiovascular and respiratory systems, despite the varied modes of activities (swimming, running, flying), different cardio-respiratory architecture, and vastly different rates of metabolism (endothermy vs. ectothermy). Our meta-analysis supports previous studies indicating a cardiovascular limit to maximal O(2) transport and also implicates a respiratory system limit to maximal CO(2) efflux, especially in ectotherms. Thus, natural selection would operate on the respiratory system to enhance maximal CO(2) excretion and the cardiovascular system to enhance maximal O(2) uptake. This provides a possible evolutionary explanation for the conundrum of why the respiratory system appears functionally over-designed from an O(2) perspective, a unique insight from previous work focused solely on O(2) fluxes. The results suggest a common gas transport blueprint, or Bauplan, in the vertebrate clade.
The objectives of this study were (1) to measure plasma (V(p)), blood (V(b)), extracellular (V(e)), and interstitial fluid (V(ist)) volumes using the same techniques; (2) to measure the rate of plasma turnover; and (3) to characterize the three important variables required to interpret transvascular flux at an organismal level (vascular compliance [C(vas)], interstitial compliance [C(ist)], and the whole-body transvascular filtration coefficient [F(c)]) in two species of anurans that differ in their capacity to regulate blood volume during dehydrational and hemorrhagic stress. The disappearance curve of Evans blue-labeled native plasma protein fitted a two-component exponential decay model for both species, indicating that plasma proteins exchanged quickly between two kinetically distinct compartments, V(p) and V(e). V(p) calculated using serial sampling times <10 min were 61.0 mL kg(-1) for Chaunus marinus and 40.5 mL kg(-1) for Lithobates catesbeiana. Plasma turnover rate was 3% of V(p) min(-1) (1.8 mL min(-1) kg(-1)) for C. marinus and 5.5% of V(p) min(-1) (2.2 mL min(-1) kg(-1)) for L. catesbeiana. Chaunus marinus also had significantly greater V(b) (84 to 53 mL kg(-1)), V(ist) (171 to 154 mL kg(-1)), and V(e) (232 to 195 mL kg(-1)) than L. catesbeiana. C(vas) was significantly greater in C. marinus (47.3 mL kPa(-1) kg(-1)) compared with L. catesbeiana (27.7 mL kPa(-1) kg(-1)). This difference reflects the interspecific differences in V(b) because vascular distensibilities are similar (0.5% kPa(-1)). There were no interspecific differences in the C(ist) (500 mL kPa(-1) kg(-1)) or F(c) (2.5 mL kg(-1) kPa(-1) min(-1) filtration calculation; 0.2-0.5 mL kPa(-1) kg(-1) min(-1) fit to volume change data). Functionally, these circulatory/interstitial exchange variables of both anuran species exemplify a circulatory system with high rates of filtration (lymph formation) and with no capacity for transcapillary fluid uptake, hence requiring substantial lymphatic return to maintain vascular volume. The large C(ist) of both species provides a capacity to store extravascular volume with little perturbation of vascular pressure, but the resulting low interstitial pressures would create difficulties for extravascular fluid return to the dorsally located lymph hearts. The principal interspecific differences of greater V(b), V(p), V(ist), and C(vas) for the more terrestrial species, C. marinus, would stabilize cardiac function during hypovolemia (e.g., hemorrhage) and increase resistance to dehydration. This is consistent with this species' enhanced capacity to manage dehydrational and hemorrhagic challenges to blood volume regulation compared to L. catesbeiana.
Physiological vagility represents the capacity to move sustainably and is central to fully explaining the processes involved in creating fine-scale genetic structure of amphibian populations, because movement (vagility) and the duration of movement determine the dispersal distance individuals can move to interbreed. The tendency for amphibians to maintain genetic differentiation over relatively short distances (isolation by distance) has been attributed to their limited dispersal capacity (low vagility) compared with other vertebrates. Earlier studies analyzing genetic isolation and population differentiation with distance treat all amphibians as equally vagile and attempt to explain genetic differentiation only in terms of physical environmental characteristics. We introduce a new quantitative metric for vagility that incorporates aerobic capacity, body size, body temperature, and the cost of transport and is independent of the physical characteristics of the environment. We test our metric for vagility with data for dispersal distance and body mass in amphibians and correlate vagility with data for genetic differentiation (F'(ST)). Both dispersal distance and vagility increase with body size. Differentiation (F'(ST)) of neutral microsatellite markers with distance was inversely and significantly (R2=0.61) related to ln vagility. Genetic differentiation with distance was not significantly related to body mass alone. Generalized observations are validated with several specific amphibian studies. These results suggest that interspecific differences in physiological capacity for movement (vagility) can contribute to genetic differentiation and metapopulation structure in amphibians.
Activity metabolism is supported by phosphorylated reserves (adenosine triphosphate, creatine phosphate), glycolytic, and aerobic metabolism. Because there is no apparent variation between vertebrate groups in phosphorylated reserves or glycolytic potential of skeletal muscle, variation in maximal metabolic rate between major vertebrate groups represents selection operating on aerobic mechanisms. Maximal rates of oxygen consumption in vertebrates are supported by increased conductive and diffusive fluxes of oxygen from the environment to the mitochondria. Maximal CO2 efflux from the mitochondria to the environment must be matched to oxygen flux, or imbalances in pH will occur. Among vertebrates, there are a variety of modes of locomotion and vastly different rates of metabolism supported by a variety of cardiorespiratory architectures. However, interclass comparisons strongly implicate systemic oxygen transport as the rate-limiting step to maximal oxygen consumption for all vertebrate groups. The key evolutionary step that accounts for the approximately 10-fold increase in maximal oxygen flux in endotherms versus ectotherms appears to be maximal heart rate. Other variables such as ventilation, pulmonary/gill, and tissue diffusing capacity, have excess capacity and thus are not limiting to maximal oxygen consumption. During maximal activity, the ratio of ventilation to respiratory system blood flow is remarkably similar among vertebrates, and CO2 extraction efficiency increases while oxygen extraction efficiency decreases, suggesting that the respiratory system provides the largest resistance to maximal CO2 flux. Despite the large variation in modes of activity and rates of metabolism, maximal rates of oxygen and CO2 flux appear to be limited by the cardiovascular and respiratory systems, respectively.
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