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AMER. ZOOL., 27:81-95 (1987) Circulatory Adaptations of Snakes to Gravity1 HARVEY B. LILLYWHITE Department of Zoology, University of Florida, Gainesville, Florida 32611 SYNOPSIS. Comparative investigations of diverse taxa of snakes demonstrate numerous adaptations for counteracting effects of gravity on the circulation, including morphological, physiological and behavioral specializations. Arboreal and terrestrial snakes that are normally subjected to stresses from gravity are characterized by relatively high arterial pressures and ability to regulate pressure by physiological adjustments of flow and flow resistance. The heart occupies an anterior position, and the arterial blood column between the heart and head is comparatively short. Terrestrial snakes characteristically possess short vascular lungs which eliminate risks of pulmonary edema due to gravity effects during vertical posture. Problems of blood pooling in peripheral systemic vasculature are counteracted by relatively non-compliant body tissue, vasomotor adjustments, and specific movements that facilitate the venous cardiac return. Anatomical valves appear to be absent from major venous channels, but gravity, acting in concert with specific features of venous morphology, can create valving actions that impede shifts of blood volume to dependent segments of these vessels. Nearly all of these characteristics are absent or deficient in several independent lineages of aquatic snakes that are far less subject to gravitational disturbance of hydrostatic pressures. Thus, snakes provide diverse and particularly useful models for examining cardiovascular adaptations to gravity, including mechanisms of function and the evolution of cardiovascular design. INTRODUCTION Snakes provide excellent models for studies of blood circulation because of their elongate body shape. This was recognized well over three centuries ago by William Harvey who utilized snakes in his experiments and demonstrations of the circulation. Yet it is in relatively recent years that renewed interest has been directed to the function as well as form of the ophidian circulatory system. We are only beginning to appreciate the utility of this system for investigating problems of cardiovascular design, function and control. In adaptive contexts, snakes are of interest not only because of their morphology but also their ecological diversification. A corollary of the long body form is that blood vessels comprise long fluid columns that are highly susceptible to disturbance of hydrostatic pressure by the influence of gravity. Both the nature and magnitude of this disturbance vary greatly depending on the size, habitat and behavior of the animal. In this paper I examine adaptations of snakes from diverse habitats for coping with gravitational stresses on the circulation. New information is presented in addition to a modest literature review on this topic. The resulting synthesis is intended to indicate the current status of knowledge and to suggest important directions for future investigations. THEORETICAL CONSIDERATIONS If a snake is inclined to a head-up position, there are two principal effects that alter hemodynamics. First, because of the change in height of the blood column, pressure will increase passively within the lower vasculature and decrease passively in the upper vasculature. Necessarily, there is a point of no pressure change, termed the hydrostatic indifferent point, and for present purposes this can be regarded as roughly the center point of the arterial blood column (Wagner, 1886). Second, because of the hydrostatic pressure gradient, blood may shift to compliant vasculature experiencing increased transmural pressures. This pooling effect is predominantly in the venous vessels and results indirectly from the induced changes 1 From the Symposium on Cardiovascular Adaptation of hydrostatic pressure. The inevitable in Reptiles presented at the Annual Meeting of the result in the absence of intervention is a American Society of Zoologists, 27-30 December reduction of venous return to the heart, 1984, at Denver, Colorado. 81 82 HARVEY B. LILLYWHITE thence reduction of cardiac output, which further decreases arterial pressures in the upper part of the body. This inevitably reduces blood flow and perfusion pressures in the head and brain. The magnitude of the problem depends on the angle of inclined posture, the length of the snake, and the extent of blood pooling in the lower body. Snakes must be able to circumvent these problems if they are to move freely in three dimensions outside of water. Two categories of adaptation are of major importance. First, barostatic reflexes are necessary to regulate arterial pressure such that cephalic blood flow is maintained during head-up posture. Second, morphological, physiological and behavioral attributes play important roles in preventing excessive displacements of blood volume when hydrostatic gradients are present along a blood column. From a comparative point of view, mechanisms that impede hydrostatic shifts of blood volume are expected to characterize terrestrial species that are most subject to disturbance of body fluids by gravity. Aquatic species do not require such adaptations because of their existence in a liquid medium. The most effective antagonist of gravity is immersion of the body in water (Gauer and Thron, 1965). Thus, in aquatic snakes the intravascular pressure gradient during vertical posture is canceled out by a similar pressure gradient in the surrounding water, and the distribution of blood volume is largely the same regardless of body position in the water column. resistance (Lillywhite and Seymour, 1978; Lillywhite and Gallagher, 1985). Head-up tilt Reflexogenic control of blood pressure during head-up posture has been examined in some detail in the semi-arboreal rat snake, Elaphe obsoleta. The following information is based primarily on studies of this species (particularly data that are discussed in more detail by Lillywhite and Gallagher, 1985). Head-up tilt displaces a significant proportion of the blood volume toward the tail and causes an immediate reduction of heart output and arterial pressure (measured at mid-body position, Fig. 1). The pressure then quickly recovers during a period of compensation which approximates events that are observed in mammals (Gauer and Thron, 1965). A new steady state is achieved in which the central arterial pressure exceeds the pretilt value, indicating that passive changes in hydrostatic pressure induced by gravity are modified by a dynamic pressure component attributable to physiological adjustments of flow and flow resistance. Studies of tiger snakes, Notechis scutatus, indicate that the magnitude and rapidity of these physiological adjustments both vary with body temperature, and the apparent optimal response occurs at temperatures preferred by active animals (Lillywhite and Seymour, 1978; Lillywhite, 1980). Shifts of blood volume in E. obsoleta reduce ventricular systemic output and total heart output by about 50% in spite of marked increases in heart rate. Stroke volume also diminishes by a little more than REGULATION OF SYSTEMIC 50%. The physiological increase of arterial ARTERIAL PRESSURE pressure can be achieved only by a considIn mammals and in snakes, regulation of erable increase in peripheral resistance blood pressure involves barostatic reflexes which is attributable to active vasoconstricinitiated by vascular mechanoreceptors tion (Lillywhite and Seymour, 1978; Liland, on a longer time course, shifts of body lywhite and Gallagher, 1985). From the fluids to preserve the blood volume (e.g., decrease in ventricular output and the conGuyton, 1978; Lillywhite and Smits, 1984; comitant increase in arterial pressure that Smits and Lillywhite, 1985). Corrections occur during tilt, one may calculate a 2-3of hydrostatic disturbances caused by grav- fold increase in total peripheral resistance. ity primarily involve short-term adjust- Measurements of regional blood flows using ments of barostatic reflexes to modify the radioactively labeled microspheres indistatus of ventricular output and peripheral cate that blood flow is reduced significantly 83 CIRCULATORY ADAPTATIONS OF SNAKES 30 i o> L ^^^^^yy^?^^^^^^^^^^^^^^ 40 30° FIG. 1. Carotid arterial blood flow (upper panel) and dorsal aortic pressure (lower panel) measured during 30° head-up tilt in a conscious Elaphe obsoleta held within a plastic tube. Blood flow responses in the dorsal aorta are generally similar to those illustrated for the carotid artery. For details of methods see Lillywhite (1985a). in visceral organs, posterior skin and posterior skeletal muscle, but does not change statistically in brain, heart and other anterior tissues. Thus, maintenance of cephalic and cerebral blood flow during head-up posture is achieved by an orchestrated response involving cardioacceleration and a selective redistribution of blood flow visa-vis vasoconstriction in gut, kidney and posterior skin and muscle. Presumably, cardiovascular adjustments to tilting are of value for the homeostatic regulation of adequate flow and perfusion pressure at the brain. If transmural pressures of vessels fall below critical values, closure of vessels leads to instability or cessation of flow (Burton, 1972). Direct measurements of critical closure have not been attempted in snakes or other reptiles, but certain observations deserve comment. Terrestrial snakes increase locomotor activity when arterial pressures fall to values below about 20 mm Hg (unpublished observations), and these levels of pressure lead to cardiorespiratory stress (Lillywhite et al., 1983). While there is considerable interspecific variation of mean arterial pressure among snakes, the lower limit of values is in the range 10-20 mm Hg (Seymour and Lillywhite, 1976; Lillywhite and Pough, 1983; Seymour, 1987). Moreover, species exhibiting the lowest values of arterial pressure inhabit aquatic environments where transmural pressures of vessels, hence perfusion pressures, are not subject E E 20 H cc 10 UJ CC 0 water a. -10 oc UJ -20 -30 air J 30 60 TILT ANGLE, 0 90 FIG. 2. Effect of tilting on cephalic arterial pressures of sea snakes, Aipysurus laevis, in air and in water. Blood pressures were measured from the dorsal aorta at mid body and corrected for the hydrostatic arterial column between the head and site of measurement. Arterial pressure of the snake in water was corrected for external water pressure by subtracting pressure of water at depth corresponding to site of measurement or calculation. The pressures shown reflect the effect of gravity acting on a continuous fluid column, although collapse of vessels in air could theoretically prevent arterial pressure from becoming negative. The dashed line depicts the expected drop of cephalic arterial pressure due solely to the passive (hydrostatic) effect of gravity on the snake tilted in air. Thus, the actual decline of pressure involves a significant component attributable to blood pooling and reduction of heart output. Original data are from Lillywhite and Pough (1983). to perturbation by gravity (Fig. 2). On the other hand, snakes that move in three dimensions outside of water (e.g., arboreal species) are characterized by much higher arterial pressures (Table 1) (Seymour and Lillywhite, 1976; Lillywhite et al., 1983). Elevated arterial pressure minimizes the probability that passive hydrostatic changes induced by head-up posture will fall to critical levels that jeopardize perfusion (Seymour and Lillywhite, 1976). From the results of tilt experiments wherein arterial pressures are measured at the body center, arterial pressures at brain 84 HARVEY B. LILLYWHITE TABLE 1. Mean arterial pressures and their control in various snakes. * Cephalic pressure during tilt, % control cm Arterial pressure, mm Hg Boiga dendrophila (3) Arboreal 126 74 75 Coluber constrictor (2) 116 42 80 161 62 58 133 47 76 Austrelaps suberbus (2) Terrestrialsemi-arboreal Terrestrialsemi-arboreal Terrestrial (climbs well) Terrestrial 66 61 80 Notechis scutatus (9) Terrestrial 93 49 71 Masticophis flagellum (1) 140 48 67 Crotalus viridis (9) Terrestrial (climbs well) Terrestrial Seymour and Lillywhite, 1976 Seymour and Lillywhite, 1976 Unpublished data 89 26 42 Unpublished data Agkistrodon piscivorus (1) Semi-aquatic 106 32 31 Unpublished data Laticauda colubnna (3) Semi-aquatic 116 Z.. semifasciata (3) Semi-aquatic 110 Cerberus rhynchops (3) Semi-aquatic 64 Acrochordus granulalus (2) Aquatic 77 Hydrophis belcheri (2) Aquatic 92 //. ornatus (3) Aquatic 97 Aipysurus laevis (2) Aquatic 111 Acalyptophis peronii (3) Aquatic 85 Emydocephalus annulatus (1) Aquatic 74 Species (n) Elaphe obsoleta (15) Piluophis melanoleucus (7) Habits Total length. * Pressures at the level of the head during 45° head-up tilt pressure. All values for n > 1 are means. level can be calculated by subtracting a hydrostatic correction from the mid-body measurement, assuming that the density of blood is 1.04 g/ml (Lillywhite and Smith, 1981). These procedures indicate that cephalic arterial pressures of E. obsoleta are usually maintained at about 50-90% of pretilt values and typically do not fall below 30 mm Hg during 45° head-up tilt (Lillywhite and Gallagher, 1985). At the other extreme, cephalic pressures of sea snakes drop to zero or become negative when they are tilted comparably outside of water (Fig. 2) (Seymour and Lillywhite, 1976; Lillywhite and Pough, 1983). The control of cephalic pressures in species from other Source of raw data Seymour and Lillywhite, 1976 Unpublished data Lillywhite and Gallagher, 1985 Unpublished data Seymour and Lillywhite, 1976 Seymour and 32 9 Lillywhite, 1976 Seymour and 35 72 Lillywhite, 1976 27 Seymour and 18 Lillywhite, 1976 Seymour and <0 33 Lillywhite, 1976 <0 22 Seymour and Lillywhite, 1976 19 sO Lillywhite and Pough, 1983 Lillywhite and 28 11 Pough, 1983 18 0 Lillywhite and Pough,1983 are expressed as percentage of the pretilt mean 38 38 environments appears to be graded according to the degree of gravitational disturbance normally encountered by animals (Table 1) (Seymour and Lillywhite, 1976). For example, control of arterial pressure in the semi-aquatic Laticauda colubrina is intermediate with respect to that observed in strictly terrestrial or aquatic snakes. Rattlesnakes appear to control blood pressure less effectively during postural changes than do other species of terrestrial snakes that are more prone to climbing. Rattlesnakes are comparatively stout and spend much of their time in horizontal postures, often in seclusion or inactivity. Terrestrial viperids as a group may 85 CIRCULATORY ADAPTATIONS OF SNAKES o> UJ 3 0 oc => 6 0 (/) pulmonary ttrleryl_ I — g 30 Q. 90i 1 Mil FIG. 3. Effects of 45" and 90° head-down tilt on systemic arterial pressure (measured in central dorsal aorta, upper panels) and pulmonary arterial pressure (measured distal to lung apex, lower panels) of a conscious Elaphe obsoleta. Tilt angles are indicated by numbers at bottom of figure. Both pressures were measured at the same level, 24% of body length from the head and anterior to the hydrostatic indifferent point. be expected to exhibit less control of blood pressure than do snakes that climb more frequently. The observed correlations between behavioral ecology and ability to control blood pressure are complicated by considerations of body length. Thus, the semiaquatic Cerberus rhynchops has relatively poor ability to increase arterial pressure during head-up tilt (Seymour and Lillywhite, 1976), yet maintains cephalic pressures relatively well because of its short body length (Table 1). Indeed, short body length may allow patterns of habitat exploitation unavailable to snakes that are long. Hence, young snakes are relatively more arboreal in habits than are the longer adults in some species (e.g., March, 1928; Test et al., 1966; Henderson et al, 1976). Further discussion of length and blood pressure in the context of gravity may be found in Seymour (1987). Head-down tilt Movements of snakes in aerial environments entail situations where the head is positioned down as well as up. In the former case the problem becomes one of perfusing the tail while avoiding excessive pressures at the head. When snakes are tilted to head-down positions there ensues a transient increase of stroke flow and central arterial pressure, systolic pressure being elevated more than the mean. Bradycardia typically follows, and the arterial pressure slowly returns toward the pretilt value (Fig. 3). The cardiovascular adjustments to headdown tilt appear to be opposite to those incurred by head-up postures, although the magnitude of bradycardia in response to head-down positions is considerably less than the magnitude of tachycardia associated with head-up positions of comparable tilt angle (Lillywhite and Seymour, 1978). In general, systemic pressures are regulated more effectively during head-up than during head-down postures (Seymour and Lillywhite, 1976; Seymour, 1987). Barostatic reflexes and arterial mechanoreceptors Barostatic reflexes have been identified in every snake that has been examined, and probably all snakes control blood pressure to some degree by means of cardiovascular mechanoreceptors. Presently, there is little information about the afferent side of blood pressure control in any reptile. Because this information has been reviewed recently, only a few comments will be noted here (seeJones and Milsom, 1982;Berger, 1987). The heart and central vasculature of all 86 HARVEY B. LILLYWHITE 1 min 30 45 FIG. 4. Effects of head-up tilt on dorsal aortic blood pressure of a conscious, bilaterally vagotomized Elaphe obsoleta. Similar results were obtained in two other vagotomized snakes. In each case, at least 5 days were allowed for postoperative recovery. Angles of tilt are indicated at bottom of panel. reptiles are richly innervated and, as in mammals, there are numerous sites that potentially monitor the mechanical status of the cardiovascular system (Boyd, 1942; Abraham, 1969; Burnstock, 1969). Morphological and physiological studies indicate that baroreceptors are located close to the heart, either in the proximal truncal region or at the base of the pulmonary artery (Fedele, 1935; Adams, 1958; Kamenskaya^a/., 1977;Berger^a/., 1980; Faraci et ai, 1982). Boyd (1942) suggested that baroreceptive regions of the snake Vipera berus might be found at the carotid bifurcation and aorta, as well as the pulmonary artery. Recordings of vagal afferent nerve activity in conjunction with vessel occlusions indicate that mechanoreceptors are located in the proximal pulmonary artery of rattlesnakes {Crotalus viridis) (Kozubowski et al., 1984). In other snakes, baroreceptive regions are thought to extend between the heart and head (Seymour and Barker, 1983). In any case, elimination of afferent nerve signals from baroreceptive regions destroys the ability of snakes to regulate blood pressure during head-up posture (Fig. 4). The occurrence of barostatic reflexes in aquatic vertebrates suggests that these mechanisms have general utility in circulatory control and did not evolve solely in response to selection pressures related to gravity (Jones and Milsom, 1982). However, studies of snakes make it clear that properties of barostatic control systems have diversified greatly as consequence of exposure to varying intensity of gravitational stresses. For example, the degree of 10Fic. 5. Pressor responses of conscious snakes to norepinephrine, injected intravenously at arrows. The aquatic Acrochordus granulatus received a dose of 100 Mg/kg (A) while the semi-arboreal Elaphe obsoleta received a dose of 10 Mg/kg (B). The hypertension induced by exogenous catecholamine in Acrochordus is about maximal for this species but is exceeded considerably in Elaphe, even at much lower doses. Pressures were recorded from indwelling, non-occluding catheters positioned within the central dorsal aorta, and doses of norepinephrine were injected in small carrier volumes of 50 ^1 saline (plus ca. 50 /il saline flush). Temperatures were 26.5°C for Acrochordus and 29.5°C for Elaphe. (Temperature differences do not account for the difference in pressor response.) cardiovascular control associated with baroreflexes of sea snakes is feeble in comparison with terrestrial species (Lillywhite and Pough, 1983). Interest arises as to which components of the reflex have been modified or have regressed as a consequence of relaxed selection (for hydrostatic adjustments) in the aquatic environment. Stimulation of cardiovascular effectors by catecholamines elevates arterial pressure in aquatic snakes, albeit not to levels that occur in terrestrial snakes (Fig. 5). With respect to tilt responses outside of water, either efferent stimulation of these effectors is small, or blood pooling (due to gravity) overwhelms the response. Pooling of blood is involved to some degree (Lillywhite, 1985ft), but the lack of pressure regulation during hemorrhage as well as tilt suggests that effector stimulation is relatively deficient in these snakes (Lillywhite and Pough, 1983). This must occur because CIRCULATORY ADAPTATIONS OF SNAKES of reduction in the number or efficacy of autonomic efferent nerve terminals, or reduction of information from the afferent (receptor) side of the reflex. Further research aimed at discriminating these possibilities could provide valuable insights for understanding the evolutionary development of baroreflex mechanisms. Attention should also be paid to possible hormonal involvement in barostatic control of blood pressure in snakes and other reptiles. Position of the heart Several aspects of ophidian morphology ar^ correlated with cardiovascular function in the context of gravity. One of the more consistent is the anatomical position of the heart. The ophidian heart is always anterior of the body center, but the position varies according to species differences in behavior and ecology. Whereas the heart occupies anterior positions in arboreal and many terrestrial snakes, it is closer to midbody in species that are aquatic (Seymour and Lillywhite, 1976; Seymour, 1987). At extremes, the heart occupies positions approaching 15% of the body length from the head in arboreal species and occurs at nearly 45% of the body length in aquatic species. Heart positions of fossorial and semi-aquatic species are intermediate. Viperid snakes appear to be exceptional in that heart position converges more toward that of aquatic snakes than other terrestrial species (discussed in Seymour, 1987). Displacement of the heart from a central location conceivably positions baroreceptors advantageously with respect to transducing hydrostatic pressure changes during movements in a vertical plane. An anterior position favors perfusion of the brain and minimizes pressure against which the heart must work when the head is up (proportional to the effective vertical distance of the blood column between heart and head). The energetic advantage of a shortened blood column in the head-up posture is compromised, however, by the lengthened venous column and reduced filling pressure at the heart. Cardiac work, for example, will increase to the extent that pumping rate is reflexly accelerated to compensate pressure for reduced venous 87 return. Furthermore, climbing entails movement in two directions, and a heart that is forward of mid-body must pump against the hydrostatic pressure of a long vascular column when the head is down. Therefore, heart position in snakes probably represents a compromise among potentially conflicting selection pressures. These include 1) proximity to a central location to minimize energy costs of perfusing vasculature distant from the heart (Seymour, 1987); 2) proximity to a central location to minimize effects of vertical posture on venous return; 3) proximity to the hydrostatic indifferent point to minimize disturbance of filling pressure at the heart; 4) proximity to the head to maximize cerebral perfusion pressures during head-up posture; 5) strategic location of baroreceptors anterior of the hydrostatic indifferent point to detect and correct shifts of hydrostatic pressures whenever postures depart from horizontal. REGULATION OF PULMONARY ARTERIAL PRESSURE Hemodynamics of the lung vasculature As in other tetrapod vertebrates, the reptilian lung is a low resistance vascular circuit, and mean pulmonary arterial pressures are generally lower than levels of systemic arterial pressure measured in the same animal (Burggren, 1977a, b; Johansen and Burggren, 1980). Pulmonary arterial pressures often exceed those of mammals while the converse is true of plasma oncotic pressure. Consequently, the reptilian lung is prone to filter relatively large amounts of fluid across highly permeable capillaries (Burggren, 1982). The extent of transcapillary filtration appears proportional to blood flow and (by inference) intracapillary pressure. Inasmuch as intrapulmonary pressures are essentially atmospheric, features of the circulation are expected to counteract the development of excessive blood pressures within the pulmonary vessels. For comparative purposes, I report pulmonary and systemic arterial pressures that were measured simultaneously in several species of snakes (Table 2). These data indicate that mean pulmonary and sys- 88 HARVEY B. LILLYWHITE TABLE 2. Mean systemic and pulmonary arterial pressures in different snakes.* Species (n) Systemic pressure, mm Hg Pulmonary pressure, mm Hg Difference, mm Hg 54 24 30 Unpublished data 41 45 31 32 43 24 29 18 16 31 17 16 13 16 12 Burggren, 1977a Burggren, 1977a Burggren, 1977a Unpublished data Unpublished data 24 12 12 Unpublished data 25 20 5 Unpublished data Source Terrestrial-semi-arboreal Elpahe obsoleta (1) Terrestrial Thamnophis radix (2) T. sirtalis (3) T. elegans (4) Crotalus viridis (2) Masticophis lateralis (1) Semi-aquatic Lalicauda colubrina (1) Aquatic Aipysurus laevis (1) * Calculated from the relation (systolic pressure + 2 diastolic pressure)/3. temic pressures are more similar in species having low systemic pressure than in species characterized by high systemic pressure. Because of the need to protect the lung from excessive intravascular pressures, the systemic hypertension that characterizes arboreal snakes must have evolved in concert with mechanisms that maintain separation of pressures on the two sides of the anatomically undivided circulation (see Burggren, 1977a). Regulation of pulmonary pressure is evident from experiments in which rat snakes (Elaphe obsoleta) are tilted head down while intravascular pressures are measured simultaneously in anterior systemic and pulmonary vessels (Fig. 3). Both pressures increase upon tilting due to the hydrostatic column and increased stroke volume as blood is displaced toward the heart. But whereas systemic pressure remains elevated, sometimes for considerable periods, there is relatively rapid adjustment that returns pulmonary pressure toward the pretilt level. Because pressures that are generated within the single ventricle influence both sides of the circulation and the pulmonary vasculature is most susceptible to damage from hypertension, advantage is seen in having barostatic mechanoreceptors in the pulmonary circuit. The interaction of controlling mechanisms for systemic and pulmonary pressures and their influence on intraventricular shunts remain to be investigated. Lung morphology and the influence of gravity Lungs of snakes conform to the ophidian body plan and are elongated structures. They are, however, divisible anatomically and functionally into several parts. Except for primitive snakes of the Boidae and Xenopeltidae, only the right lung is developed, and the left lung is rudimentary or absent (Butler, 1895). Thus, in the majority of snakes the lung is a single large axial chamber. Gas exchange takes place through membranous walls of radial chambers (termed faveoli by Duncker, 1978). These surround the central lumen of the respiratory organ and give a faviform appearance to the wall of the lung. This region is highly vascular, and, for purposes of the present discussion, this respiratory structure will be referred to as vascular lung (McDonald, 1959). Posteriorly, respiratory parenchyma may be absent, and the lung continues for variable distances as saccular lung which is a simple, blind-ending sac. The saccular lung is relatively avascular and its wall is usually a thin, membranous sheet (but may be thick and muscular in sea snakes). Anteriorly, the trachea is often a ventral groove that opens into variable amounts of vascular parenchyma or joins with membranous wall to form a simple but expandable tube. The open trachea with respiratory parenchyma have been called tracheal lung (Beddard, 1903), and will here be treated as specialized vascular lung. Fur- CIRCULATORY ADAPTATIONS OF SNAKES 89 FIG. 6. Schematic drawing illustrating differences of lung morphology in snakes that are differentially exposed to hydrostatic stresses from gravity. Position of the heart is indicated in solid black, the extent of vascular lung is depicted by cross-hatching, and the total lung is outlined in black. For purposes of illustrating relative differences, all snakes are drawn to a common length. (A) Acrochordus granulatus, aquatic; (B) Laticauda colubrina, semi-aquatic; (C) Crotalus viridis, terrestrial but is not prone to climb; (D) Elaphe obsoleta, terrestrial and semi-arboreal. Each drawing is based on quantitative measurements (unpublished data). Further comparisons (largely qualitative) of lung morphology may be found in Brongersma (1951); Varde (1951); George and Shah (1956); Tenney and Tenney (1970); Kardong (1972a, A); Read and Donnelly (1972); Graham et al. (1975); Glass and Johansen (1976); Donnelly and Woolcock (1977); Gratz et al. (1981); Luchtel and Kardong (1981). ther details of pulmonary morphology can be found in various references (e.g., Wolf, 1933; Varde, 1951; Frenkel and Kochva, 1970; Luchtel and Kardong, 1981). While the entire lung extends a considerable distance of the body length, the proportional length of vascular lung varies greatly in different snakes (Fig. 6). In totally aquatic snakes the vascular parenchyma extends virtually the entire length of the lung and body cavity, except in species having a short saccular segment. In contrast, vascular lungs of arboreal and many terrestrial snakes are proportionally very much shorter and may occupy less than 20% of the body length. Lungs of rattlesnakes are intermediate, and the vascular segment extends as tracheal lung from the heart anterior to the head. These differences in morphology have significance for gravity effects on hydrostatic pressures and pulmonary function. Both the pulmonary artery and pulmonary vein characteristically extend the entire length of the faveolar tissue and delimit the vascular lung. Therefore, pulmonary vessels comprise fluid columns that vary in length according to habitat and risk of hydrostatic disturbance. The long pulmonary vessels of aquatic snakes potentially develop significant hydrostatic pressures, if they are positioned vertically in air. Because these pressures develop in both arterial and venous columns, they are transmitted to capillaries and the lung is at risk of severe edema. To demonstrate the effects of body position on the intravascular pressures of a long vascular lung, I tilted sea snakes (Aipysurus laevis) head-up in air while measuring pressures from indwelling catheters positioned within posterior segments of the pulmonary vessels. As expected, tilting a snake to progressively greater angles of head-up posture increases pressure stepwise in both the pulmonary artery and pulmonary vein 90 HARVEY B. LILLYWHITE (Fig. 7). Venous pressures can be regarded as representative of intracapillary pressures and almost certainly produce edema, assuming that colloid osmotic pressures are lower than those in mammals (Burggren, 1982). Histological examination of lung tissue taken from A. laevis soon after tilting reveals swollen tissue, congested blood vessels, and presence of red blood cells in faveolar spaces outside of capillaries (unpublished observations). Such conditions might contribute to the listless behavior and deaths that occur after sea snakes are tilted in air (Lillywhite and Pough, 1983). Normally, of course, gravity will not greatly affect the pulmonary transmural pressures of aquatic snakes because counteracting pressures in the external water column collapse lung segments and increase air pressure in the remaining segments that contain compressed gas. On the other hand, evolution of a short vascular lung in terrestrial snakes confers the advantage of avoiding the gravity problem in air. A short pulmonary blood column appears to be a consistent feature of arboreal and terrestrial species of snakes and suggests that length is a real morphological constraint on the function of reptilian lungs in threedimensional aerial environments. Advantages of the elongated respiratory organ of aquatic snakes are not established. Clearly, radial diffusion distances are reduced in comparison with more complex parenchyma of terrestrial snakes in which the total exchange surface is contained within a much shorter length of organ. Faveoli comprise about 16% of the lung radius in a sea snake (Seymour et al., 1981) compared with 55% of the vascular lung radius in a python (Read and Donnelly, 1972; Donnelly and Woolcock, 1978). Inasmuch as long vascular lungs are functionally improbable in aerial environments, the radially elaborate pulmonary structure of terrestrial snakes is likely a simple consequence of compensating surface area for reduced length of the organ. T H E PROBLEM OF VENOUS RETURN The subject of venous return has been a neglected topic in cardiovascular studies of reptiles. Notwithstanding this defi- ciency, the hemodynamics of venous return to the heart takes on particular significance for long-bodied snakes, especially in the contexts of gravity and vertical position. Central venous pressures in horizontal snakes are characteristically near zero or from one to several mm Hg positive (Lillywhite and Smith, 1981; Lillywhite, 1985a; unpublished data). Pressures within the vena cava of rat snakes (E. obsoleta) increase in response to circulating catecholamines (unpublished data) and remain virtually constant during graded arterial hemorrhage (Lillywhite and Smith, 1981). These data imply that venous tone is actively regulated in these snakes, so venoconstriction is likely to play a role in promoting venous return in various circumstances. Presumably, movement of blood to atria and central veins is always assisted by ventricular contractions that reduce intrapericardial pressures and promote a vis afronte phase of cardiac filling (Johansen and Burggren, 1984). Blood pooling and postural edema The return of blood to the heart through veins is jeopardized by the venous compliance which allows distension of vessels and displacements of blood volume when snakes are subjected to the gravitational influence of head-up postures. The extent of blood pooling in caudal vasculature is proportional to the tilt angle and varies considerably in different species of snakes (Lillywhite, 19856). Blood pooling in aquatic species and in rattlesnakes is 3-10-fold greater than in arboreal and semi-arboreal species (including arboreal viperids) and thus correlates inversely with ability to control arterial pressure during tilt. Tissue plethysmography and measured reductions of circulating blood volume during tilt indicate that gravity increases the capillary filtration of plasma and thus contributes to edema of tissues in addition to the pooling of whole blood (Lillywhite, 19856 and unpublished data). Thus, the extent to which blood volume is displaced to dependent tissues in different species probably reflects variability of capillary permeability as well as compliance of vessels and the interstitial space. Measurements of trans- 91 CIRCULATORY ADAPTATIONS OF SNAKES Venous valves: Do they exist? The advantages of valves in the context of gravity are twofold: first, valves prevent 40- : B DC 1 -:-L a. - • •'•] i • P -— -— — • 20 — 0 • 45 J --- • "1 capillary shifts of fluid in snakes subjected to hemorrhage or exercise suggest that capillary permeability is relatively great, particularly in sea snakes (Lillywhite and Pough, 1983; Lillywhite and Smits, 1984; Smits and Lillywhite, 1985). Species of snakes that pool small quantities of blood are also characterized by relatively high arterial pressures, whereas species that are prone to pool larger quantities of blood have lower and poorly regulated pressures. Thus, neglecting differences in length, the latter species exhibit greater distension of dependent tissue per unit of arterial pressure. Assuming that venous pressures are comparable in snakes of identical length, the compliance of body tissues appears to be considerably less in species that regulate arterial pressure effectively than in those that are prone to pool blood and regulate pressure poorly. The foregoing conclusion is supported by the heterogeneity of morphology that is observed in various taxa. For example, many snakes that are specialized for arboreal life have slender bodies, and the integument is tightly coupled to underlying tissue. Assuming that the Laplace principle applies in some form to the integument or body wall of snakes, the slender body shape of arboreal species is structurally advantageous for counteracting edema and pooling of blood in tissues (notwithstanding other ecological benefits such as camouflage). In contrast, rattlesnakes and various aquatic species of snakes have a more flaccid body structure and loosely coupled integument. Because all of these snakes may ingest bulky meals, the compliance of the integument and outer body wall cannot be related solely to feeding habits. Thus, it is plausible that aspects of gross morphology and mechanical features of tissues are adaptations or preadaptations to counteract the effects of gravity on body fluids. Venous architecture and differences in the level and control of venous tone might also be expected to correlate with the gravitational environment of species. -m Hrr 6C 1 9( —* G FIG. 7. Arterial (A) and venous (B) pressures measured in posterior segments of pulmonary vessels of sea snakes (Aipysurus laevis) during head-up tilting in air. Numbers at lower panel of figure indicate angles of tilt. Arterial and venous pressures were measured in two different snakes (respective lengths = 103 and 108 cm). retrograde flow of blood and, second, they provide discontinuities within a vertical venous column, thereby reducing hydrostatic pressures in the lower body of the animal. I am unaware of published descriptions of anatomical valves in the larger venous channels of any snake, although they are reported to occur in lymphatics (Ottaviani and Tazzi, 1977). Accordingly, I examined blood-filled veins in freshly killed snakes with the objective of testing for presence of anatomical valves. Tests involved 1) moving blood back and forth by applying pressure gently with wet fingers, 2) tilting the snake on a tilt board and observing displacements of blood, 3) injecting a bubble of air into a catheterized vessel and following the movement of the bubble along a vessel in a retrograde direction, and 4) advancing a catheter tip gradually through vessels in directions away from the heart. The vessels examined were pulmonary vein, precaval and jugular veins, 92 HARVEY B. LILLYWHITE postcaval, portal and renal veins. I exam- rhynchops, which strengthens the suggesined both terrestrial and aquatic species tion that it functions as a gravitational valve. including five Elaphe obsoleta, one Pituophis The hypothetical occurrence of bidirecmelanoleucus, one Agkistrodon contortrix, andtional gravitational valves instead of unithree Acrochordus granulatus. Blood moved directional valves seems advantageous to freely retrograde in all of the snakes, indi- long-bodied snakes because such struccating that valves were either absent from tures could impede blood pooling regardor non-functional in the veins that were less of whether the body posture is headexamined. While valves may be present in up or head-down. Furthermore, body smaller branches of the venous system, movements of snakes (as in climbing) probblood is clearly free to move in either direc- ably act alternately to create or eliminate tion within the larger (and longer) venous valve effects, possibly under conscious conchannels of these snakes. trol (see below). Although internal valves of the form familiar from mammalian studies appear Lymphatics to be absent from the great veins of snakes, The lymphatic system of snakes is highly retrograde movement of venous blood can developed and extensively embraces the be impeded by configurations of vessels in major blood vessels (Chapman and Conkspecific circumstances. The following lin, 1935; Ottaviani and Tazzi, 1977). Periexamples are situations that I have noted vascular and paravascular lymphatic chanduring the performance of surgery and nels course for long distances in snakes numerous dissections (Fig. 8). 1) Localized (unpublished observations) and conceivconstrictions of vascular smooth muscle are ably act like "water jackets" to stabilize occasionally noted to impede blood move- transmural pressures to an unknown degree ment, probably due to localized trauma during vertical posture. The organization, associated with disturbance of vessels. Sys- compliance and hydrostatic behavior of temic veins of E. obsoleta are capable of such lymphatic structures clearly invite increasing tone dramatically in response to comparative and detailed examination in circulating catecholamines, so it is con- the various ophidian taxa. ceivable that some form of tonus valving due to myogenic or neurogenic mecha- The role of behavior nisms impedes blood pooling in circumVirtually any body movement potenstances of postural disturbance of hydro- tially affects hemodynamics of the ophidstatic pressures. 2) Hairpin loops of vessels ian circulation. Ventilatory movements can trap blood if sufficient volume impinges compress and expand venous channels, suddenly at the wall of the loop. 3) In ter- thereby influencing venous pressures and restrial snakes the segment of portal vein the flow of blood toward the heart (Johanimmediately posterior to the liver (and sen and Burggren, 1984; Lillywhite, sometimes within the posterior aspect of 1985a). In the snake Elaphe obsoleta, arteliver) is twisted in the manner of a cork- rial pressures vary as much as 12 mm Hg screw for distances of several centimeters. during individual breathing cycles and The corkscrew appearance is attributable sometimes increase by nearly twice this to helical fascia applied to the outer wall amount if ventilatory depth is altered over of the vessel and anchored obliquely to several breathing cycles (Lillywhite, 1985a). adjacent tissue. During head-up tilt of Thus, increased ventilation observed dursnakes on a tilt board, blood sometimes ing head-up posture (Lillywhite and Galdams up in the helices of the corkscrew lagher, 1985) or during hemorrhage (Lilwhich subsequently impedes retrograde lywhite et al., 1983) may improve blood flow. This structure conceivably acts bidi- flow in addition to facilitating gas exchange rectionally, although I have observed valv- at the lung. ing effects only in the one direction. The Locomotor movements elevate blood corkscrew structure is absent in the aquatic pressure by directly compressing vessels snakes Acrochordus granulatus and Cerberus and, more importantly, increasing venous CIRCULATORY ADAPTATIONS OF SNAKES 93 £50 | 30 o? 1 0 _?20r 10 1 min FIG. 8. Hypothetical valves created by forces of gravity acting on major systemic veins of snakes. The direction of gravity displacement is indicated by the arrow, and the density of stippling indicates trapped blood. Each functional valve depends on structure external to the lumen of the vessel. Each valve action has been observed in fresh tissues of dissected snakes; further study is required, however, to confirm the actions of these valves in naturally active and undisturbed snakes. (A) Localized myogenic or neurogenic contraction of vascular smooth muscle narrows vessel lumen to near occlusion. (B) Retrograde movement traps blood in loop of vessel, and the expanding vessel wall creates occlusion at the site of entrapment. (C) Retrograde movement traps blood in a "pocket" of vessel wall created by helical turns and corkscrew shape of vessel. return and ventricular output (Lillywhite, 1985a). Although locomotor activity reduces blood volume due to transcapillary shifts of filtered plasma (Lillywhite and Smits, 1984)—an effect that is facilitated by gravity—the tendency for blood pressure to fall is counteracted by the behaviorally improved status of venous return. Species of snakes that are normally subjected to gravity in aerial environments behaviorally increase venous return and ventricular output to improve the arterial FIG. 9. Effects of body movements on carotid arterial blood flow (upper panel), aortic pressure (middle panel) and central venous pressure (lower panel) of an adult rat snake (Elaphe obsoleta). Asterisks at lower panel indicate the occurrence of undulatory movements induced by previously hemorrhaging a part of the blood volume. (From Lillywhite [1985a] with permission from University of Chicago Press.) pressure (Fig. 9). Arboreal and terrestrial snakes employ what I have termed "cardiovascular facilitative movements" to counteract gravitational or experimentally induced hypotension (Lillywhite, 1985a). Such movements consist of lateral undulations that move rapidly along the body length independently of locomotion and characteristically in an anterior direction. They are associated with climbing or the assumption of vertical postures in the wild and can also be induced by rendering a snake hypotensive in the laboratory. The movements are observed in terrestrial and arboreal species, but are neither observed nor induced in aquatic species. Although other body movements also increase arterial pressures, stereotyped cardiovascular facilitative movements are relatively more effective and presumably evolved specifically to assist the blood circulation. The evolution of such specializations in arboreal snakes emphasizes the necessity to maintain cardiovascular competency dur- 94 HARVEY B. LILLYWHITE ing vertical posture and climbing. (The movements specialized to maintain blood pressure should not be confused with locomotion or swaying movements that presumably assist vision or evade predators.) CONCLUSION In summary, snakes that move in vertical dimensions of aerial environments are characterized by a number of attributes that are deficient or lacking in species that do not routinely experience the hydrostatic stresses of gravity. Characteristics of the former group of snakes include 1) high arterial pressure, 2) ability to regulate blood pressure by barostatic adjustments of flow and flow resistance, 3) anterior position of the heart and presumptive locations of baroreceptive regions that are cephalad to the hydrostatic indifferent point of the circulation, 4) reduced length of vascular lung and associated pulmonary vessels, 5) presumptive morphological and physiological mechanisms to impede blood pooling in venous vasculature and tissues, including 6) relatively low-compliant body wall and integument, and 7) behavioral specializations to promote the return of venous blood to the heart. These cardiovascular traits may be regarded as adaptive because they are convergent in diverse taxa of independent lineages and correlate more closely with behavior and ecology than phylogenetic history. 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