THE JOURNAL OF EXPERIMENTAL ZOOLOGY 275:217-226 (1996)

Gravity, Blood Circulation, and the Adaptation of Form and Function in Lower Vertebrates
HARVEY B. LILLYWHITE Department of Zoology, University of Florida, Gainesville, Florida 32611
ABSTRACT Gravitational force influences musculoskeletal systems, fluid distribution, and hydrodynamics of the circulation, especially in larger terrestrial vertebrates. The disturbance to hydrodynamics and distribution of body fluids relates largely to the effects of hydrostatic pressure gradients acting in vertical blood columns. These, in turn, are linked to the evolution of adaptive countermeasures involving modifications of structure and function. Comparative studies of snakes suggest there are four generalizations concerning adaptive countermeasures to gravity stress that seem relevant to lower vertebrates generally. First, increasing levels of regulated arterial blood pressure are expected to evolve with some relation to gravitational stresses incurred by the effects of height and posture on vertical blood columns above the heart. Second, aspects of gross anatomical organization are expected to evolve in relation to gravitational influence incurred by habitat and behavior. Third, natural selection coupled to gravitational stresses has favored morphological features that reduce the compliance of perivascular tissues and provide an anatomical antigravity suit. Fourth, natural selection has produced gradients or regional differences of vascular characteristics in tall or elongated vertebrates that are active in high gravity stress environments. Consideration or awareness of these principles should be incorporated into interpretations of struc@ 1996 Wiley-Liss, Inc. ture and function in lower vertebrates.

Vertebrates are derived from marine ancestors, and their subsequent evolution involved adaptive radiations and development of primitive body plans in aquatic environments (McFarland e t al., 85). At present, nearly half of the extant vertebrates are aquatic and include some of the earliest as well as diverse and successful taxa, represented by the fishes. The adaptive radiation of aquatic vertebrates occurred in a liquid environment where buoyancy provides virtual weightlessness. Successful living on land, however, subjected organisms t o increasing influence of gravitational force and demanded considerable modifications in the design and function of gravity-sensitive structures.

AQUATIC VS. TERRESTRIAL ENVIRONMENTS

Because the density of blood and water are nearly the same, gradients of hydrostatic pressure in vertical blood columns are counterbalanced by virtually equal gradients of pressure in surrounding water (Fig. 1).Therefore, transmural pressures remain approximately constant, and the distribution of blood volume does not change when animals change posture or orientation. Thus, the fundamental design of the early vertebrate circulation evolved in relation to demands for nutrient
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distribution, gas exchange, and other factors, while gravity was not of foremost significance. Gravity does affect marine and deep fresh water organisms indirectly by virtue of the high pressures that develop with depth. However, there appears t o be no information that reliably points to differences of cardiovascular characters between vertebrates exposed t o low and high pressures. Because of the effects of high pressures on chemical reaction volumes and enzyme function (Somero, 921, hydrostatic pressures associated with benthic habitats probably influence functional designs of the heart, vascular muscle and endothelium at molecular and cellular levels. These features, however, appear not t o be reflected in gross anatomy of the vertebrate circulation. In terrestrial environments gravity profoundly influences musculoskeletal anatomy, fluid distribution, and the neural regulation of these systems. Hydrostatic pressure is an important component of blood pressure, and its contribution increases with the height of a blood column. Taller animals are more directly affected by gravity in this context, such that gravity-sensitive taxa include

Address reprint requests Dr. H.B. Lillywhite, Department of Zoology, The University of Florida, Gainesville, FL 326114525,

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ADAPTIVE COUNTERMEASURESTO GRAVITY STRESS ON THE CIRCULATION

Intuitively, intravascular gradients of gravitational pressure do not pose a significant problem for most terrestrial lower vertebrates due to their small size. A large number of vertebrate species are smaller than 100 g, and this is especially true for ectothermic taxa. For example, nearly 80% of the species of amphibians and lizards weigh less than 20 g, and many weigh less than 5 g (Pough, '83).Of course, slender and elongated body forms having low mass-to-length ratios are not exempt from considerable hydrostatic pressures while in vertical positions. Such vertebrates have not been well investigated in contexts of gravity and circulation, however. Considering the larger species of lower vertebrates, most research investigations that are relevant to a gravitational context have involved snakes. In the subsequent sections of this article, data based largely on research investigations of snakes will be discussed with the view of formulating several conclusions regarding gravitational adaptation in lower vertebrates generally.

Fig. 1. Schematic representation of a hypothetical blood column illustrating gradients of hydrostatic pressures depicted by arrows. The size of the arrows corresponds to the magnitude of the pressure vectors. In aqueous environments hydrostatic pressures outside the blood column increase with depth approximately as do hylirostatic pressures within the blood column, such that trarismural pressures across the boundary (e.g., vessel wall) remain unchanged along the column length. In aerial environments the arrows outside the blood column represent atmot3pheric pressure which virtually does not change along the length of the column. The wall forming the boundary which contains the blood is assumed t o be compliant, such that increasing gradients of transmural pressure in air cause distension and blood pooling in the lower depths of the blood column.

ARTERIAL BLOOD PRESSURE: GRAVITY AND SAFETY FACTORS

Lower vertebrates are, with few exceptions, ectothermic, and they display generally lower levels of activity and body temperature than are characteristic of endothermic birds and mammals. As a consequence, systemic arterial pressures are generally lower than those which characterize the cardiovascular systems of the endothermic vertebrates. Systemic pressures reported for fishes, amphibians and reptiles are typically less than 40 mm Hg, and many are less than 30 mm Hg (Burggren e t al., in press). Exceptions include tuna, salmon, crocodilians, varanid lizards and arboreal snakes, all of which may have systemic pressures similar to those in mammals (Burggren et al., in press). The higher levels of arterial pressure appear to have evolved in relation t o the metabolic demands of activity (fishes, varanids), separation of systemic and pulmonary circulation (crocodilians and varanids), and the gravitational demands of the habitat (snakes, possibly varanids). Mean resting arterial blood pressure is significantly correlated with body mass in snakes (Seymour, '87) but also tends t o be higher in arboreal species and lower in aquatic and nonclimbing species irrespective of size (Seymour and Lillywhite, '76; Seymour, '87). Resting arterial

mammals, long-necked o r long-legged birds, caecilians, and certain reptiles such as snakes, large lizards, crocodilians and extinct dinosaurs. The principle problem created by gravity vectors which are acting parallel to the length of the body is the increase in Fressure in the lower aspect of fluid columns (Fig. 1).This effect potentially elevates capillary filtration pressures which promote tissue edema, but can be opposed by vasoconstriction at the upstream side of capillaries. More significantly, increased pressures distend vessels, especially the compliant storage vessels of the venous system. The effect promotes pooling of blood in dependent vasculature and reduces venous return to the heart, thereby decreasing cardiac filling. The tendency for cardiac output t o decrease under these conditions reduces arterial filling and, because the stressed vascular volume is diminished, contributes to decreased arterial pressures required to move blood against gravity (Seymour et al., '93). Natural selection for countermeasures to gravitational stress on blood circulation largely involves itraits that are associated with these linked problems.

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pressures in arboreal species range generally between 40 and 90 mm Hg, whereas those in aquatic or amphibious species are generally between 18 and 30 mm Hg, The differences in arterial pressure between scansorial and nonscansorial species also correlate with abilities t o maintain central arterial pressure during head-up posture outside of water (Fig. 2). Thus, in comparison with aquatic or ground-dwelling species (Lillywhite and Pough, 83; Lillywhite, 93a), scansorial species are characterized by relatively high resting arterial pressure and superior control of arterial pressure in relation to gravitational perturbations of hemodynamics (Lillywhite and Gallagher, 85; Lillywhite, 87). Proximate reasons for the higher arterial pressures in scansorial snakes are no doubt complex, but are likely related primarily to differences in

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Fig. 2. Graph showing arterial blood pressure in snakes from different gravitational environments and how they change during head-up tilt. Pressures are measured at the body center and so are not expected t o exhibit passive change if the arterial column acted as a hypothetical fluid contained within a rigid tube (see Gauer and Thron, 65). The increase of pressure during tilt in arboreal species is attributable t o physiological regulation which elevates central pressure t o compensate for the passive decrease in pressure a t the head. The decrease of pressure during tilt in the aquatic species is attributable to blood pooling in the lower body which overwhelms comparatively feeble physiological controls. Data are based on Lillywhite and Donald (941, a s modified from Seymour and Lillywhite (76).

characteristic levels of peripheral resistance. In terms of ultimate causes, higher arterial pressure is decidedly advantageous as a countermeasure to gravity stress insofar as it helps ensure adequate perfusion of the head and cerebral vasculature at all attitudes of posture (Seymour and Lillywhite, 76; Lillywhite, 87). Consider two snakes which have comparable hydrostatic blood columns above the heart when the body is vertical with the head up. Both animals experience an identical passive drop of pressure at the upper end of the vascular column (due solely t o gravitys effect on hydrostatics) while in the upright posture. However, the snake with the higher arterial pressure has a larger margin of safety before the fall in pressure jeopardizes the perfusion hemodynamics at the head, regardless of whether a siphon effect assists the blood flow during upright posture. Clearly, the heart must develop a pressure exceeding that of the hydrostatic column above it in order to open the outflow valves and produce (or maintain) flow (see also Seymour et al., 93).Arterial blood pressure in snakes appears t o be directly related to the distance between the heart and head of terrestrial species (Seymour, 87). Indeed, it has been possible to demonstrate that carotid arterial blood flow becomes null when the arterial pressure measured at heart level decreases to a value just below that required t o support the blood column above the heart (Fig. 3). Similarly, data from terrestrial mammals indicate that levels of systemic arterial pressure exceed those of the hydrostatic column above the heart when the animals are in a standing position. Thus, there is a crude correlation between the characteristic arterial blood pressure and height of larger terrestrial mammals (Patterson et al., 75). In consideration of the above, it appears that increasing levels of arterial pressure are expected to evolve with some relation to the degree of gravitational stress which a species experiences as a result of its height and postural behavior. Secondarily, other traits which are linked to blood pressure must coevolve with the level of arterial pressure. Thus, heart mass scales t o the 0.95 power in snakes but only 0.77 t o 0.91 in other reptiles which are not as subject to gravitational stress (Seymour, 87). Increasingly higher systemic pressures create a potential problem in terms of excessive pulmonary pressures, inasmuch as the ventricle is single and the pulmonary and systemic circuits are anatomically undivided in noncrocodilian lower vertebrates. Therefore, evolution of higher systemic

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CARDIOVASCULAR
MECHANORECEPTORS AND GROSS ANATOMICAL ORGANIZATION
Regulation of arterial pressure involves a number of interacting control systems in probably all vertebrates. A prominent control system, and perhaps the most important control of blood pressure during acute disturbance related t o posture change, is the baroreceptor reflex. Baroreflexes are present in all groups of lower vertebrates, including fishes (Burggren et al., in press). Their presence in aquatic fishes emphasizes their utility in nongravitational contexts and the fact that their evolution was not associated with factors related to gravity stress. The available comparative information indicates that, as in mammals, there are multiple baroreceptor sites in the central vasculature of probably most species. The efferent side of the baroreflex activates cardiac activity and the constrictory tone of vascular smooth muscle. Limited data suggest that efferent responses might be more effective in gravitychallenged species (cf. Lillywhite and Pough, '83; Lillywhite and Gallagher, '85).However, little information is available t o compare the gain of baroreflexes in species that are subject to different degrees of gravitational stress. Baroreceptor sites in snakes occur in association with arterial outflow tracts adjacent t o the heart (Lillywhite and Donald, '94). The heart has an anterior position in gravity-challenged species (Seymour and Lillywhite, '76; Seymour, '87; Lillywhite, '87), so baroreceptors are positioned with enhanced capacity t o detect changes of pressure or vascular distension (Jones and Milsom, '82). In addition to cardiovascular mechanoreceptors located centrally near the heart, there probably are vascular mechanoreceptors in peripheral vasculature. Clearly it is quite possible that sensory inputs to cardiovascular reflexes involve such peripheral receptors which probably exhibit differential distributions in variably gravity-sensitive species. Other aspects of morphology differ between scansorial, gravity-sensitive species and nonscansorial species of snakes. Such characters include, in addition to heart position, length of the vascularized (functional) lung, body length, body girth or slenderness, and proportional length of the tail (Lillywhite, '87, '88). Thus, there is the expectation that there is evolutionary reorganization of gross anatomical features in species which are subjected t o

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Fig. 3. Simultaneous measurements of carotid arterial blood flow and dorsal aortic pressure measured with reference to heart level in a rat sn,ske, Elaphe obsoleta. The ability of this particular snake t o regulate arterial pressure has been compromised by loss of blood volume due t o experimental hemorrhage. The segment cif record illustrates the dynamic responses t o 30" head-up tilt, beginning at the arrow. Note that carotid blood flow decreases t o zero when arterial pressure is reduced to a level (indicated by horizontal dashed line) where the pressure at the heart equals that of the hydrostatic column above the heart. The record indicates that the ventricle must produce a pressure in excess of the hydrostatic column above it in order to produce flow in the cephalad direction. Reproduced from Lillywhite and Donald ('94), with permission.

pressures necessitated the coevolution of some mechanism or suite of factors which maintains separation of pressures in the two circuits of the blood circulation. Pulmoinary arterial pressures in snakes are maintained generally below 20 mm Hg in spite of a broad range of resting systemic pressures in various species (Lillywhite and Donald, ' 9 4 ) .Presumably, separation of pressures in the two circuits involves resistance adjustments in the extrinsic (proximal) pulmonary arteries and (or) functional separation of ejection pressures from the ventricle, as in Varcznus spp. (Heisler et al., '83). Birds and mammstls evolved separation of systemic and pulmonary blood flows by means of an anatomically divided ventricle, so further evolution of increased levels of arterial pressure was not as problematic.

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gravitational stresses related to variation of habi-

Shape

Arboreal snakes are typically very slender, with ratios of circumference-to-length being considerably smaller than those of other confamilial species (Lillywhite and Henderson, '93). The slender shape is advantageous because a smaller circumference provides greater resistance to a given disTHE PROBLEM OF BLOOD POOLING: tending force than does a larger circumference, EVOLUTION OF AN "ANTIGRAVITY SUIT" reflecting the principle of the Law of Laplace. EvoThe principal problem associated with upright lution of an elongated tail allometry mentioned posture is pooling of blood in dependent vasculaabove also confers the advantage of this principle, ture and the attendant reduction of venous reirrespective of other selective pressures that might turn to the heart. The problem is well illustrated have possibly provided the evolutionary driving by the "orthostatic intolerance" of nonscansorial force producing the long tail. snakes, including both aquatic and certain grounddwelling terrestrial species. When these snakes Low compliance tissues are tilted to head-up positions, carotid blood flow ceases at tilt angles between 30" and 45" (LillyScansorial species of snakes exhibit tendencies white, '93a). This inability t o maintain carotid to reduced caudal blood pooling during upright blood flow during upright posture has been corre- posture. The magnitude of change in tail volume lated with tendencies to blood pooling and ineffec- attributable to the combined pooling of blood and tual vasomotor control of peripheral vasculature filtered plasma varies from about 1% in arboreal (Lillywhite and Pough, '83; Lillywhite, %a, '93b). species t o 9% in aquatic species during head-up How do snakes that have adopted arboreal or tilt in air (Lillywhite, '85a). Such differences in climbing habits avoid the problem of blood pool- blood pooling might be attributable to morphologiing? Three factors appear to have particular im- cal attributes as well as to vasomotor status of portance with respect to this question: these are the resistance and capacitance vessels. The mesize, shape and compliance of the extravascular chanical properties of snake skin are complex and space surrounding blood vessels in dependent vas- depend on factors other than skin thickness or culature. patterns of scalation (Jayne, '88). Comparative data from Jayne's study do not allow generalizaSize tions about mechanical attributes of the skin of The majority of scansorial snakes have evolved scansorial species. However, allowing for differwithin three families: Boidae, Colubridae and Vi- ences in thickness, skin from a species of arboperidae. With few exceptions, the arboreal spe- real snake was shown to have greater stiffness cies tend t o be relatively short when compared than that of the nonarboreal species tested, sugwith related members of the same family, many gesting there are differences in the dermal colaveraging less than 1m in length (Lillywhite and lagen fibers or some other feature which remains Henderson, '93). Arboreal colubrids may be longer, to be identified. In spite of variation in mechanibut these species are characterized by a propor- cal properties of integument per se, the complitionately long tail, sometimes comprising more ance of subcutaneous compartments depends also than 40% of the total body length. This latter fea- on how tightly the skin is applied t o the underlyture has probable significance for gravitational ing tissue. Indeed, the integument of scansorial hemodynamics because the caudal tissues of species appears to have tighter and more extensnakes provide a much tighter extravascular en- sive attachment to underlying tissues than does vironment for blood vessels than does the body that of nonscansorial species (Lillywhite and cavity (Lillywhite and Henderson, '93). Smits, '92; Lillywhite and Henderson, '93). Thus, Many arboreal lower vertebrates (such as frogs compliance of the subcutaneous tissue space was and lizards) are quite small, and the length of their found to be greater in aquatic and nonscansorial vascular columns when upright does not limit the species than in scansorial species of snakes postural requirements of arboreal habits. Longer (Lillywhite, '93b). Presumably, such differences of species (for example varanid lizards) presumably compliance reflect adaptive structural modificahave modifications affecting compliance of tissues tions related t o requirements for counteracting which limit blood pooling, as in snakes. gravitational stresses in the various forms. Fiform, snakes probably reflect this principle in more exaggerated ways than are apparent in other vertebrate species. Some of the relevant features are discussed in further detail below.

tat and behavior. Because of their attenuate body

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nally, based on whole body volume/pressure relations in vivo, the vasculature in aquatic file snakes (Acrochordus urufurue)is about three times more compliant than that of terrestrial pythons (Liasis fuscus; Arndt and Seymour, 93). These whole body measurements presumably incorporate the stiffness of vessels as well as the surrounding body tissues of the snake. The combined morphological characters which limit vascular expansion might be referred t o appropriately as an anatomical antigravity suit. The importance of such a feature to gravitational hemodynamics is illustrated by experimental data from a semiaquatic snake (Nerodia rhornbiferu) which was restrained within a tight-fitting tube during exposure to graded increases of acceleration force produced in the head-to-tail direction (G,) on a centrifuge (Lillywhite et al., 96). The tight tube prevented expansion of the snakesbody and thereby increased the level of acceleration which the snake could withstand (from +2 t o +3 G,) without cessation of carotid arterial blood flow. Evidently, this change of response reflects a substantial increase in the cardiovascular tolerance to G, force due solely to the mechanical countenneasure, without attendant (changesin physiology. Whether morphological characteristics described here for scansorial snakes have evolved in other lower vertebrates as countermeasures to gravity is not known. However, these features in snakes appear t o be convergeint with those of upright mammals. Giraffes, for example, have very tight skin investing the feet and legs which help t o counteract gravitationa I edema that might otherwise arise from the high levels of blood pressure that prevail in the dependent limbs of such tall animals (Hargens et al., 87, 88).Aquatic animals do not require such features because the surrounding water column provides a passive, external antigravity suit. Thus, natural selection associated with gravitational stress favors tightness of external anatomy and extravascular tissues which thereby provide an antigravity wit. A summary of these features in snakes is depicted in Figure 4.

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Fig. 4. Comparisons of blood pooling in the circulatory systems of (A) a generalized arboreal snake, (B) a nonclimbing terrestrial snake, and (C) an aquatic snake. Blood pooling is constrained by morphology and low compliance of perivascular tissues in the arboreal snake, and by the liquid environment external to the aquatic snake. Relatively compliant tissues of the nonclimbing terrestrial snake allow considerable pooling of blood during hypothetical periods of upright posture. These examples assume static conditions. Movements and behavior can mitigate pooling in all species, but are more effective in the arboreal forms (cf. Lillywhite, 85b, 93a). Reproduced from Lillywhite and Henderson (93), with permission.

BLOOD VESSELS P L N D GRADIENTS OF VASCULAR ADAPTATION The foregoing discussion brings us to the subject of the blood vessels Ibemselves. Ophidian vasculature bears adrenergic innervation which varies interspecifically in patterns that are correlated with the behavior and habitat of species. Arboreal and other scansorial species have especially

dense innervation of major arteries and veins posterior to the heart, whereas anterior vessels are innervated more sparsely (Donald and Lillywhite, 88, 95). Furthermore, an extensive distribution and colocalization of neuropeptides in perivascular nerves innervating the larger arteries and veins also indicate there is functional specialization within components of the peripheral autonomic system controlling the circulation, especially with regard to regulation of venous capacity (Davies and Donald, 92).The patterns suggest there has been considerable adaptive modification in the distribution of perivascular autonomic nerves to the larger blood vessels of snakes in relation to gravitational

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demands that were imposed during their evolutionary history. Neurally mediated regulation of vascular resistance and capacity is of primary importance in contexts of homeostatic responses to gravitational stress (Lillywhite and Seymour, '78). Regional changes of blood flow during head-up posture have been investigated by means of radiolabeled microsphere distribution in semiarboreal rat snakes (Lillywhite and Gallagher, '85). Blood flow t o heart, lung and brain was shown t o be regulated, while there was pronounced vasoconstriction and reduced blood flow in splanchnic organs and posterior skin and muscle. Thus, cerebral blood flow is maintained by these regional adjustments of flow and resistance, in combination with central shunts that redirect flow in a cephalad direction (Lillywhite and Donald, '88). The major venous pathways lack valves in many snakes that have been examined (Lillywhite, '871, and the posterior veins of rat snakes bear an especially dense innervation (Donald and Lillywhite, '88). These observations suggest that neurogenic regulation of venous capacity may be of particular importance in scansorial species of snakes (Lillywhite and Donald, '94). Recently the larger blood vessels of rat snakes were shown to be reactive to vasoactive agonists in specific anatomic patterns related to the gravitational demands of climbing (Conklin et al., '96). In particular, catecholamines stimulate severalfold greater tension in posterior than in anterior vessels, which were shown t o have lesser inherent contractility in vitro (Fig. 5 ) . Such data provide functional correlates of innervation patterns which most likely evolved in relation to gravitational influence on postural hemodynamics. Thus, natural selection has produced gradients or regional differences of vascular characteristics along the body length of elongate vertebrates which are active in high G-stress environments. Other examples of such regional adaptation include gradients of capillary basement membrane thickness which increases twofold from neck muscle to leg muscle of adult giraffes and humans (Williamson et al., '71). Such membranes in the human fetus are uniform and considerably thinner than those in children or adults. Regional responses to local differences of hydrostatic pressure are also evident in the variation of medial smooth muscle (Goetz and Keen, '57; Pettersson et al., '86) and innervation (Nilsson et al., '88) of giraffe blood vessels. Similar or novel examples might also be expected among ectothermic vertebrates but have not been widely investigated.

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Fig. 5. Maximal tension development of arterial segments in relation to anatomical distribution of blood vessels in the rat snake, Eluphe obsoleta. Data are shown for mean (2S.E.) maximal responses of vascular smooth muscle to norepinephrine. (Responses to epinephrine and 80 mM potassium are both qualitatively and quantitatively similar.) Vessel abbreviations: ADA, anterior dorsal aorta; CA, carotid artery; MDA, midbody dorsal aorta; PDA, posterior dorsal aorta. Data from Conklin et al. ('96).

The condition of structural and functional gradients related to gravity adaptation raises some interesting considerations. For example, there is currently great interest in the role of endothelium in regulating blood flow and resistance in vessels. The question arises, is an endothelial cell an endothelial cell, or might endothelial properties vary according t o regional hemodynamics related to gravity? Clearly, the possibility of regional variation in functional properties of endothelium should be considered in the planning of experiments or the interpretation of data from different species of animals. Gravitational factors may well contribute to the functional variability that is present.

CONCLUSIONS In summary, we might expect to find adaptive variation of form and function in various vertebrates experiencing variable exposure to gravitational stresses. Extreme modifications such as those seen in snakes are related t o size, posture, behavioral activities, and terrestriality. Studies of snakes indicate that gravity has: (1)influenced the evolution of arterial pressure and its regulation; (2) determined, in part, the placement and form of internal organs such as heart and lung; (3) constrained body length in certain environments; (4) led t o modifications of body shape and compliance of subcutaneous compartments affect-

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mechanism of intracardiac shunting in the lizard Varanus exanthematicus. J. Exp. Biol., 105:15-31. Jayne, B.C. (1988) Mechanical behavior of snake skin. J. Zool. (Lond.), 214:125-140. Jones, D.R., and W.K. Milsom (1982) Peripheral receptors affecting breathing and cardiovascular function in non-mammalian vertebrates. J. Exp. Biol., 100:59-91. Lillywhite, H.B. (1985a) Postural edema and blood pooling in snakes. Physiol. Zool., 58:759-766. Lillywhite, H.B. (198513) Behavioral control of arterial pressure in snakes. Physiol. Zool., 58:159-165. Lillywhite, H.B. (1987) Circulatory adaptations of snakes to gravity. Am. Zoologist, 27:81-95. Lillywhite, H.B. (1988) Snakes, blood circulation and gravity. Sci. American, 256:92-98. Lillywhite, H.B. (1993a) Orthostatic intolerance of viperid snakes. Physiol. Zool., 66:lOOO-1014. Lillywhite, H.B. (1993b) Subcutaneous compliance and gravitational adaptation in snakes. J. Exp. Zool., 267: 557-562. Lillywhite, H.B., and J.A. Donald (1988) Anterograde bias of blood flow in arboreal snakes. Am. Zoologist, 28:86A. Lillywhite, H.B., and J.A. Donald (1994) Neural regulation of arterial blood pressure in snakes. Physiol. Zool., 67r12601283. Lillywhite, H.B., and K.P. Gallagher (1985) Hemodynamic adjustments to head-up posture in the partly arboreal snake, Elaphe obsoleta. J. Exp. Zool., 235:325-334. Lillywhite, H.B., and R.W. Henderson (1993) Behavioral and functional ecology of arboreal snakes. In: Snakes: Ecology and Behavior. R. Seigel and J. Collins, eds. MacMillan, New York, pp. 1-48. Lillywhite, H.B., and F.H. Pough (1983) Control of arterial pressure in aquatic sea snakes. Am. J. Physiol., 244:R66R73. Lillywhite, H.B., and R.S. Seymour (1978) Regulation of arterial blood pressure in Australian tiger snakes. J. Exp. Biol., 75~65-79. Lillywhite, H.B., and A.W. Smits (1992) The cardiovascular adaptations of viperid snakes. In: Biology of the Pitvipers. J.A. Campbell and E.D. Brodie, Jr., eds. Selva, Tyler, pp. 143-153. Lillywhite, H.B., R. Ballard, and A.R. Hargens (1996) Tolerance of snakes to hypergravity. Physiol. Zool., 69293-303. McFarland, W.N., F.H. Pough, T.J. Cade, and J.B. Heiser (1985) Vertebrate Life, 2nd edition. MacMillan Publishing Company, New York. Nilsson, O., S. Booj, A. Dahlstrom, A.R. Hargens, R.W. Millard, and K.S. Pettersson (1988) Sympathetic innervation of the cardiovascular system in the giraffe. Blood Vessels, 25:299307. Patterson, J.L., Jr., R.H. Goetz, J.T. Doyle, J.V. Warren, O.H. Gauer, D.K. Detweiler, S.I. Said, H. Hoernicke, M. McGregor, E.N. Keen, M.H. Smith, Jr., E.L. Hardie, M. Reynolds, W.P. Flatt, and D.R. Waldo (1975) Cardiorespiratory dynamics in the ox and giraffe, with comparative observations on man and other mammals. Ann. NY Acad. Sci., 127:393-413. Pettersson, K., A.R. Hargens, R.W. Millard, K Johansen, D.H. Gershuni, R. Burroughs, D.G.A. Meltzer, and W. van Hoven (1986) Dependent hypertension and arterial wall hypertrophy without interstitial oedema in the giraffe. Proc. Int. Union Physiol. Sci., 16:411.

ing blood vessels; (5) influenced structure, compliance and function of blood vessels; and (6) created gradients or regional variation of structure and function within the body. For gravitational biologists who might be interested in applied aspects of gravity adaptation, such as countermeasures to space travel, lower vertebrates such as snakes might provide important material for investigations into basic mechanisms and processes related to gravitational effects. Whether or not gravitational effects are the focus, studies of vertebrate structure and function should be approached and interpreted with an awareness of the generalizations that have been summarized herein.

ACKN0W:LEDGMENTS Writing of this review, and part of the work on which it is based, were undertaken with support from NASA and the National Research Council while the author was a. Resident Associate at the Ames Research Center, Moffett Field, California. LITERATURE CITED
Amdt, J.O., and R.S. Seymour (1993) Adaptation of the cardiovascular system to gravity: Volume/pressure relations of the circulation of terrestrial and aquatic snakes. Abstract 90.15P of 32nd I.U.P.S. Congress, Glasgow. Burggren, W.W., A.P. Farrell, and H.B. Lillywhite (1996) Vertebrate cardiovascular systems. In: Handbook of Comparative Physiology. W. Dantz ler, ed. American Physiological Society, Bethesda, Maryland (in press). Conklin, D.J., H.B. Lillywhite, K.R. Olson, R.E. Ballard, and A.R. Hargens (1996) Blood vessel adaptation to gravity in a semi-arboreal snake. J. Comp. Physiol., B165:518-526. Davies, P.J., and J.A. Donald (1992) The distribution and colocalization of neuropeptides in perivascular nerves innervating the large arteries and veins of the snake, Elaphe obsoleta. Cell Tissue Res., 269:495-504. Donald, J.A., and H.B. Lillyv, hite (1988) Adrenergic innervation of the large arteries and veins of the semiarboreal rat snake Elaphe obsoleta. J. Morph., 198:25-31. Donald, J.A., and H.B. Lillywhite (1995) Adrenergic innervation of the larger arteries and veins of snakes. Faseb J., 9:A354. Gauer, O.H., and H.L. Thron (1965) Postural changes in the circulation. In: Handbook of Physiology, Sec. 2, Circulation, Vol. 3. W.F. Hamilton and P. Dow, eds. American Physiological Society, Washington, D.C., pp. 2409-2439. Goetz, R.H., and E.N. Keen (1957) Some aspects of the cardiovascular system in the giraffe. Angiology, 8:542-564. Hargens, A.R., R.W. Millard, I<. Pettersson, and K. Johansen (1987) Gravitational haemodynamics and oedema prevention in the giraffe. Nature, 32959-60. Hargens, A.R., D.H. Gershuni, L.A. Danzig, R.W. Millard, and K. Pettersson (1988) Tissu~sadaptations t o gravitational stress: Newborn versus adult giraffes. Physiologist, 31:SllOS113. Heisler, N., P. Neumann, arid G.M.O. Maloiy (1983) The

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