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Mass Transport: Circulatory System with Emphasis on Nonendothermic Species

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ABSTRACT

Mass transport can be generally defined as movement of material matter. The circulatory system then is a biological example given its role in the movement in transporting gases, nutrients, wastes, and chemical signals. Comparative physiology has a long history of providing new insights and advancing our understanding of circulatory mass transport across a wide array of circulatory systems. Here we focus on circulatory function of nonmodel species. Invertebrates possess diverse convection systems; that at the most complex generate pressures and perform at a level comparable to vertebrates. Many invertebrates actively modulate cardiovascular function using neuronal, neurohormonal, and skeletal muscle activity. In vertebrates, our understanding of cardiac morphology, cardiomyocyte function, and contractile protein regulation by Ca2+ highlights a high degree of conservation, but differences between species exist and are coupled to variable environments and body temperatures. Key regulators of vertebrate cardiac function and systemic blood pressure include the autonomic nervous system, hormones, and ventricular filling. Further chemical factors regulating cardiovascular function include adenosine, natriuretic peptides, arginine vasotocin, endothelin 1, bradykinin, histamine, nitric oxide, and hydrogen sulfide, to name but a few. Diverse vascular morphologies and the regulation of blood flow in the coronary and cerebral circulations are also apparent in nonmammalian species. Dynamic adjustments of cardiovascular function are associated with exercise on land, flying at high altitude, prolonged dives by marine mammals, and unique morphology, such as the giraffe. Future studies should address limits of gas exchange and convective transport, the evolution of high arterial pressure across diverse taxa, and the importance of the cardiovascular system adaptations to extreme environments. © 2017 American Physiological Society. Compr Physiol 7:17‐66, 2017.

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Figure 1. Figure 1. A conceptual view of the relationship between resting oxygen (O2) consumption and body size, establishing two “zones.” In the zone to the lower left below the dashed line, simple diffusion of gases, nutrients, and wastes is adequate for either very small organisms (e.g., protists and worms) or the exceptional larger, but relative inactive animals (flatworms). In the upper right zone, internal blood convection is required for larger animals (vertebrates) or the exceptional very active smaller animals (e.g., Daphnia).
Figure 2. Figure 2. A model for pressure/flow stimulation of angiogenesis in the early vertebrate embryo. Panel A shows the hemodynamic factors of flow‐ and pressure‐generating cyclic and shear stress on the endothelium‐lined walls of the vasculature. Panel B shows the response of individual endothelial cells to hemodynamically generated stressors. Secretion of VEGF through a paracrine effect stimulates division of adjacent endothelial cells. Adapted, with permission, from (83).
Figure 3. Figure 3. The relationship between embryo size (as radius) at the onset of convective blood flow (r onset) and the calculated maximum embryo radius at which diffusion can serve O2 uptake needs (r max). Four vertebrate classes with highly varying rates of O2 consumption are represented. The “synchronotropy line” (dashed line) indicates the point in this interrelationship at which there is a perfect match between the onset of blood flow and the development of the need for blood flow for O2 transport. The solid line represents a regression through the plotted data points. See text and (80) for additional details of the calculations and their interpretation.
Figure 4. Figure 4. Endothelial vascular lining, blood pressure, and the major animal lineages. The appearance of a complete or incomplete endothelial vascular lining is shown, along with an indication of general blood pressures for each group. Downward arrow indicates low blood pressure; upward arrow indicates high blood pressure. Adapted, with permission, from (83).
Figure 5. Figure 5. Mechanisms of cardiac regulation. (A). Intrinsic cardiac regulation: The neurogenic decapod heart contracts in response to pacemaker cells associated with the cardiac ganglion located in or on the dorsal aspect of the heart. These interneurons synapse with larger motoneurons that innervate cardiac muscle fibers directly and through extensive dendritic ramifications control both rate and strength of cardiac contractions. Extrinsic cardiac regulation: The cardiac ganglion, myocardia, ostia, suspensory ligaments, and arterial valve are all under extrinsic neuronal and neurohormonal control. The rate and force of cardiac contraction are modulated through cardioregulatory nervous input to both the cardiac ganglion and myocardia. Through the thoracic ganglion (dorsal nerve) two pair of cardio accelerator nerves (SN III) and one pair of cardio inhibitor nerves (SN II) influence the rate of depolarization of the pacemaker cells in the cardiac ganglion and force of myocardia contraction. Neurohormonal control of cardiac function is through the pericardial organ (PO), which releases an array of cardioactive substances into the paricardial sinus in response to dorsal nerve input via the neuroregulatory fibers. (B) Cardiac contraction is initiated by the cardiac ganglion, resulting in the generation of tension and myocardial contraction. The myocardia is composed of a three‐dimensional array of fibers arranged around the lumen of the heart (B3) and forces hemolymph into multiple arterial systems through the arterial valves (B2). Both nervous regulate arterial and ostial valve tone and neurohormonal input to facilitate coordinated and functional contraction (B1). B1 adapted, with permission, from (6), B2 and B3 adapted, with permission, from (369).
Figure 6. Figure 6. The functional linkage between the actions of the cardiac ganglion and the generation of hemolymph pressure to drive blood through the circulatory system is myocardial contraction. The decapod (Procambarus clarkii) cardiac cycle begins with systole, isovolumic contraction (muscle fiber depolarization with the generation of pressure or tension) as seen by the rapid rise in intracardiac pressure which rapidly igoes from close to zero to approximately 1.33 kPa. A notch similar to the dicrotic notch seen in mammalian ventricular pressure profiles is observed as the multiple arterial valves open due to the ventricular‐arterial pressure difference. Intracardiac and arterial pressures equalize once the arterial valves are open and hemolymph is propelled out of the ventricle into the arteries during the ejection phase. Arterial pressures are maintained above intracardiac pressure once the arterial valves close and the heart goes into isovolumic relaxation. Arterial hemolymph pressure diminishes slowly due to the passive elastic properties of the major vessels leaving the heart. Diastole or ventricular filling occurs as the result of a pericardial‐intracardiac pressure difference. During diastole, pericardial pressure continues to increase as hemolymph moves from the infrabranchial sinus through the gills and into the pericardial region. Open ostial valves allow the pressure difference to drive hemolymph into the ventrical during the filling phase, which ends with onset of the next systolic contrition (478).
Figure 7. Figure 7. A comparative scheme of the sources of activator Ca2+ during excitation‐contraction coupling in mammalian (A) and teleost (B) ventricular myocytes. Both cardiomyocytes are approximately the same length, but the teleost cell is narrower, elliptical in cross section, lacks transverse tubules, has a less well‐developed SR, and has a much higher surface area to volume ratio. Contractile activity in all vertebrate hearts depends, in large part, on how much Ca2+ is delivered, to myofilaments. In the mammalian cardiomyocyte, activator Ca2+ comes from extracellular Ca2+ entering the cell through Ca2+ channels (DHPR, #1 and 2) and Na+/Ca2+ exchangers (reverse mode, #3) on the sarcolemma and transverse tubules (T tubules). Ca2+ influx also triggers Ca2+ release from the SR (intracellular Ca2+ store) by the RyR (#4). Relaxation occurs by SR Ca2+ pumps (SERCA, #6), sarcolemmal Ca2+ pumps (#7), and Na+/Ca2+ exchangers (#8). The primary source of Ca2+ for contraction in the teleost cardiomyocyte is extracellular with transsarcolemmal influx through Ca2+ channels (#1) or Na+/Ca2+ exchangers (#2) in reverse mode. Depending on the fish species and environmental conditions, SR Ca2+ may also be important (#4). For relaxation, teleosts rely on sarcolemmal Ca2+ pumps (#5), Na+/Ca2+ exchangers (#6), and possibly SR Ca2+ pumps (#7). Based on information in references (40, 528, 593). See text for additional details.
Figure 8. Figure 8. A list of known regulators of ventricular function during a cardiac cycle in vertebrates. Although blood is shown as red, reflecting complete oxygenation, the vertebrate ventricle may pump different degrees of oxygenated or deoxygenated blood. See text for details.
Figure 9. Figure 9. Summary of diving specializations in a generic seal species.
Figure 10. Figure 10. Summary of features aiding to high‐altitude flight in bar‐headed goose either as avian general traits (blue boxes) or species‐specific specializations (orange boxes). Reprinted from (509) with permission.
Figure 11. Figure 11. Summary of specializations to account for gravitational effects in the cardiovascular system of the giraffe.


Figure 1. A conceptual view of the relationship between resting oxygen (O2) consumption and body size, establishing two “zones.” In the zone to the lower left below the dashed line, simple diffusion of gases, nutrients, and wastes is adequate for either very small organisms (e.g., protists and worms) or the exceptional larger, but relative inactive animals (flatworms). In the upper right zone, internal blood convection is required for larger animals (vertebrates) or the exceptional very active smaller animals (e.g., Daphnia).


Figure 2. A model for pressure/flow stimulation of angiogenesis in the early vertebrate embryo. Panel A shows the hemodynamic factors of flow‐ and pressure‐generating cyclic and shear stress on the endothelium‐lined walls of the vasculature. Panel B shows the response of individual endothelial cells to hemodynamically generated stressors. Secretion of VEGF through a paracrine effect stimulates division of adjacent endothelial cells. Adapted, with permission, from (83).


Figure 3. The relationship between embryo size (as radius) at the onset of convective blood flow (r onset) and the calculated maximum embryo radius at which diffusion can serve O2 uptake needs (r max). Four vertebrate classes with highly varying rates of O2 consumption are represented. The “synchronotropy line” (dashed line) indicates the point in this interrelationship at which there is a perfect match between the onset of blood flow and the development of the need for blood flow for O2 transport. The solid line represents a regression through the plotted data points. See text and (80) for additional details of the calculations and their interpretation.


Figure 4. Endothelial vascular lining, blood pressure, and the major animal lineages. The appearance of a complete or incomplete endothelial vascular lining is shown, along with an indication of general blood pressures for each group. Downward arrow indicates low blood pressure; upward arrow indicates high blood pressure. Adapted, with permission, from (83).


Figure 5. Mechanisms of cardiac regulation. (A). Intrinsic cardiac regulation: The neurogenic decapod heart contracts in response to pacemaker cells associated with the cardiac ganglion located in or on the dorsal aspect of the heart. These interneurons synapse with larger motoneurons that innervate cardiac muscle fibers directly and through extensive dendritic ramifications control both rate and strength of cardiac contractions. Extrinsic cardiac regulation: The cardiac ganglion, myocardia, ostia, suspensory ligaments, and arterial valve are all under extrinsic neuronal and neurohormonal control. The rate and force of cardiac contraction are modulated through cardioregulatory nervous input to both the cardiac ganglion and myocardia. Through the thoracic ganglion (dorsal nerve) two pair of cardio accelerator nerves (SN III) and one pair of cardio inhibitor nerves (SN II) influence the rate of depolarization of the pacemaker cells in the cardiac ganglion and force of myocardia contraction. Neurohormonal control of cardiac function is through the pericardial organ (PO), which releases an array of cardioactive substances into the paricardial sinus in response to dorsal nerve input via the neuroregulatory fibers. (B) Cardiac contraction is initiated by the cardiac ganglion, resulting in the generation of tension and myocardial contraction. The myocardia is composed of a three‐dimensional array of fibers arranged around the lumen of the heart (B3) and forces hemolymph into multiple arterial systems through the arterial valves (B2). Both nervous regulate arterial and ostial valve tone and neurohormonal input to facilitate coordinated and functional contraction (B1). B1 adapted, with permission, from (6), B2 and B3 adapted, with permission, from (369).


Figure 6. The functional linkage between the actions of the cardiac ganglion and the generation of hemolymph pressure to drive blood through the circulatory system is myocardial contraction. The decapod (Procambarus clarkii) cardiac cycle begins with systole, isovolumic contraction (muscle fiber depolarization with the generation of pressure or tension) as seen by the rapid rise in intracardiac pressure which rapidly igoes from close to zero to approximately 1.33 kPa. A notch similar to the dicrotic notch seen in mammalian ventricular pressure profiles is observed as the multiple arterial valves open due to the ventricular‐arterial pressure difference. Intracardiac and arterial pressures equalize once the arterial valves are open and hemolymph is propelled out of the ventricle into the arteries during the ejection phase. Arterial pressures are maintained above intracardiac pressure once the arterial valves close and the heart goes into isovolumic relaxation. Arterial hemolymph pressure diminishes slowly due to the passive elastic properties of the major vessels leaving the heart. Diastole or ventricular filling occurs as the result of a pericardial‐intracardiac pressure difference. During diastole, pericardial pressure continues to increase as hemolymph moves from the infrabranchial sinus through the gills and into the pericardial region. Open ostial valves allow the pressure difference to drive hemolymph into the ventrical during the filling phase, which ends with onset of the next systolic contrition (478).


Figure 7. A comparative scheme of the sources of activator Ca2+ during excitation‐contraction coupling in mammalian (A) and teleost (B) ventricular myocytes. Both cardiomyocytes are approximately the same length, but the teleost cell is narrower, elliptical in cross section, lacks transverse tubules, has a less well‐developed SR, and has a much higher surface area to volume ratio. Contractile activity in all vertebrate hearts depends, in large part, on how much Ca2+ is delivered, to myofilaments. In the mammalian cardiomyocyte, activator Ca2+ comes from extracellular Ca2+ entering the cell through Ca2+ channels (DHPR, #1 and 2) and Na+/Ca2+ exchangers (reverse mode, #3) on the sarcolemma and transverse tubules (T tubules). Ca2+ influx also triggers Ca2+ release from the SR (intracellular Ca2+ store) by the RyR (#4). Relaxation occurs by SR Ca2+ pumps (SERCA, #6), sarcolemmal Ca2+ pumps (#7), and Na+/Ca2+ exchangers (#8). The primary source of Ca2+ for contraction in the teleost cardiomyocyte is extracellular with transsarcolemmal influx through Ca2+ channels (#1) or Na+/Ca2+ exchangers (#2) in reverse mode. Depending on the fish species and environmental conditions, SR Ca2+ may also be important (#4). For relaxation, teleosts rely on sarcolemmal Ca2+ pumps (#5), Na+/Ca2+ exchangers (#6), and possibly SR Ca2+ pumps (#7). Based on information in references (40, 528, 593). See text for additional details.


Figure 8. A list of known regulators of ventricular function during a cardiac cycle in vertebrates. Although blood is shown as red, reflecting complete oxygenation, the vertebrate ventricle may pump different degrees of oxygenated or deoxygenated blood. See text for details.


Figure 9. Summary of diving specializations in a generic seal species.


Figure 10. Summary of features aiding to high‐altitude flight in bar‐headed goose either as avian general traits (blue boxes) or species‐specific specializations (orange boxes). Reprinted from (509) with permission.


Figure 11. Summary of specializations to account for gravitational effects in the cardiovascular system of the giraffe.
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Dane A. Crossley, Warren W. Burggren, Carl L. Reiber, Jordi Altimiras, Kenneth J. Rodnick. Mass Transport: Circulatory System with Emphasis on Nonendothermic Species. Compr Physiol 2016, 7: 17-66. doi: 10.1002/cphy.c150010