Journal of Experimental Zoology Part a Ecological Genetics and Physiology Volume 275 Issue 2-3 1996...

7/28/2019 Journal of Experimental Zoology Part a Ecological Genetics and Physiology Volume 275 Issue 2-3 1996 [Doi 10.100

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THE J OURNAL OF EXPERIMENTALZOOLOGY 275:217-226 (1996)

Gravity, Blood Circulation, and the AdaptationofFormand Function in Lower VertebratesHARVEY B. LILLYWHITEDepartment of Zoology, Universityof F lorida, Gainesvil le, F lorida 32611

ABSTRACT Gravitational force influences musculoskeletal systems, fluid distribution, and hy-drodynamics of the circulation, especially in larger terrestrial vertebrates. The disturbance tohydrodynamics and distribution of body fluids relates largely to the effectsof hydrostatic pressuregradients acting in vertical blood columns. These, in turn, are linked to the evolution of adaptivecountermeasures involving modificationsof structure and function. Comparative studiesof snakessuggest there are four generalizations concerning adaptive countermeasures to gravity stress thatseem relevant to lower vertebrates generally. First, increasing levels of regulated arterial bloodpressure are expected to evolve with some relation to gravitational stresses incurred by the effectsof height and posture on vertical blood columns above the heart. Second, aspects ofgrossanatomi-cal organization are expectedto evolve in relation to gravitational influence incurred by habitatand behavior. Third, natural selection coupled to gravitational stresses has favored morphologicalfeatures that reduce the complianceof perivascular tissues and provide an anatomical antigrav-ity suit. Fourth, natural selection has produced gradientsor regional differencesof vascular char-acteristics in tall or elongated vertebrates that are active in high gravity stress environments.Consideration or awarenessof these principles should be incorporated into interpretationsof struc-ture and function in lower vertebrates. @ 1996Wiley-Liss, I nc.

Vertebrates are derived from marine ancestors,and their subsequent evolution involved adaptiveradiations and development of primitive bodyplans in aquatic environments (McFarland etal., 85).At present, nearly half of the extantvertebrates are aquatic and include some of theearliest as well as diverse and successful taxa,represented by the fishes. The adaptive radia-tion of aquatic vertebrates occurred in a liquidenvironment where buoyancy provides virtualweightlessness. Successful living on land, however,subjected organisms to increasing influence ofgravitational force and demanded considerablemodifications in the design and function of grav-ity-sensitive structures.

AQUATIC VS. TERRESTRIALENVIRONMENTSBecause the density of blood and water arenearly the same, gradients of hydrostatic pressurein vertical blood columns are counterbalanced byvirtually equal gradients of pressure in surround-ing water (Fig. 1).Therefore, transmural pres-sures remain approximately constant, and thedistributionof blood volume does not change whenanimals change posture or orientation. Thus, thefundamental design of the early vertebrate circu-lation evolved in relation to demands for nutrient

0 1996WILEY-LI SS, INC.

distribution, gas exchange, and other factors,while gravity was not of foremost significance.Gravity does affect marine and deep fresh wa-ter organisms indirectly by virtue of the high pres-sures that develop with depth. However, thereappears to be no information that reliably pointsto differences of cardiovascular characters betweenvertebrates exposedto low and high pressures. Be-cause of the effects of high pressures on chemicalreaction volumes and enzyme function (Somero,921,hydrostatic pressures associated with benthichabitats probably influence functional designs ofthe heart, vascular muscle and endothelium atmolecular and cellular levels. These features, how-ever, appear not to be reflected in gross anatomyof the vertebrate circulation.In terrestrial environments gravity profoundlyinfluences musculoskeletal anatomy, fluid distri-bution, and the neural regulation of these systems.Hydrostatic pressure is an important componentof blood pressure, and its contribution increaseswith the height of ablood column. Taller animalsare more directly affected by gravity in this con-text, such that gravity-sensitive taxa include

Address reprint requests Dr. H.B. Lillywhite, Departmentof Zool-ogy, TheUniversity of Florida, Gainesville, FL 326114525,


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218 H.B. LILLYWHITEWATER AIR

Fig. 1. Schematic representation of a hypothetical bloodcolumn illustrating gradients of hydrostatic pressures depictedby arrows. The size of the arrows corresponds to the magni-tude of the pressure vectors. In aqueous environments hy-drostatic pressures outside the blood column increase withdepth approximately as do hylirostatic pressures within theblood column, such that trarismural pressures across theboundary (e.g., vessel wall) remain unchanged along the col-umn length. In aerial environments the arrows outside theblood column represent atmot3pheric pressure which virtu-ally does not change along the lengthof the column. The wallforming the boundary which contains the blood is assumedto be compliant, such that increasing gradients of transmu-ral pressure in air cause distension and blood pooling in thelower depthsof the blood column.

mammals, long-neckedor long-legged birds, cae-cilians, and certain reptiles suchassnakes, largelizards, crocodilians and extinct dinosaurs.The principle problem created by gravity vec-tors which are acting parallel to the length of thebody is the increase in Fressure in the lower as-pect of fluid columns (Fig. 1).This effect poten-tially elevates capillary filtration pressures whichpromote tissue edema, but can be opposed by vaso-constriction at the upstream side of capillaries.More significantly, increased pressures distendvessels, especially the compliant storage vesselsof the venous system. The effect promotes pool-ing of blood in dependent vasculature and reducesvenous return to the heart, thereby decreasing car-diac filling. The tendency for cardiac outputto de-crease under these conditions reduces arterialfilling and, because the stressed vascular volumeis diminished, contributes to decreased arterialpressures required to move blood against gravity(Seymour et al., '93).Natural selection for coun-termeasures to gravitational stress on blood cir-culation largely involves itraitsthatare associatedwith these linked problems.

ADAPTIVE COUNTERMEASURES TOGRAVITY STRESS ON THE CIRCULATIONIntuitively, intravascular gradients of gravita-tional pressure do not posea significant problemfor most terrestrial lower vertebrates dueto their

small size. A large number of vertebrate speciesare smaller than 100 g, and this is especially truefor ectothermic taxa. For example, nearly 80%ofthe species of amphibians and lizards weigh lessthan 20g, and many weigh less than 5g (Pough,' 83). Of course, slender and elongated body formshaving low mass-to-length ratios are not exemptfrom considerable hydrostatic pressures while invertical positions. Such vertebrates have not beenwell investigated in contexts of gravity and circu-lation, however.Considering the larger species of lower verte-brates, most research investigations that are rel-evant to a gravitational context have involvedsnakes. In the subsequent sections of this article,data based largely on research investigations ofsnakes will be discussed with the view of formu-lating several conclusions regarding gravitationaladaptation in lower vertebrates generally.ARTERIAL BLOOD PRESSURE: GRAVITYAND SAFETY FACTORSLower vertebrates are, with few exceptions, ec-tothermic, and they display generally lower lev-

els of activity and body temperature than arecharacteristicof endothermic birds and mammals.As aconsequence, systemic arterial pressures aregenerally lower than those which characterize thecardiovascular systems of the endothermic verte-brates. Systemic pressures reported for fishes,amphibians and reptiles are typically less than40 mm Hg, and many are less than 30 mm Hg(Burggren et al., in press). Exceptions includetuna, salmon, crocodilians, varanid lizards and ar-boreal snakes, all of which may have systemic pres-sures similar to those in mammals (Burggren etal., in press). The higher levels of arterial pressureappear to have evolved in relation to the metabolicdemands of activity (fishes, varanids), separationof systemic and pulmonary circulation (crocodiliansand varanids), and the gravitational demands of thehabitat (snakes, possibly varanids).Mean resting arterial blood pressure is signifi-cantly correlated with body mass in snakes(Seymour, '87) but also tends to be higher in ar-boreal species and lower in aquatic and non-climbing species irrespective of size (Seymour andLillywhite, ' 76 ; Seymour, '87). Resting arterial


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GRAVITY ADAPTATION IN LOWER VERTEBRATES 219pressures in arboreal species range generally be-tween40and90mm Hg, whereas those in aquaticor amphibious species are generally between 18and 30 mm Hg, The differences in arterial pres-sure between scansorial and nonscansorial spe-cies also correlate with abilities to maintaincentral arterial pressure during head-up postureoutside of water (Fig.2).Thus, in comparisonwithaquaticor ground-dwelling species (Lillywhite andPough, 83;Lillywhite, 93a), scansorial species arecharacterized by relatively high resting arterialpressure and superior control of arterial pressurein relation to gravitational perturbations of he-modynamics (Lillywhite and Gallagher, 85; Lilly-white, 87).Proximate reasons for the higher arterial pres-sures in scansorial snakes are no doubt complex,but are likely related primarily to differences in

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lot0 1 1 1 1 1 1 1 1 1 1 10 10203040 50 6070 80 90

Tilt angleFig. 2. Graph showing arterial blood pressure in snakesfrom different gravitational environments and how theychange during head-up tilt. Pressures are measured at thebody center andsoare not expectedto exhibit passive changeif the arterial columnactedas ahypothetical fluid containedwithin a rigid tube (see Gauer and Thron, 65).The increaseof pressure during tilt in arboreal species is attributable tophysiological regulation which elevates central pressure tocompensate for the passive decrease in pressure at the head.The decrease of pressure during tilt in the aquatic species isattributable to blood pooling in the lower body which over-whelms comparatively feeble physiological controls. Data arebased on Lillywhite and Donald (941,as modified fromSeymour and Lillywhite(76).

characteristic levels of peripheral resistance. Interms of ultimate causes, higher arterial pressureis decidedly advantageous as a countermeasureto gravity stress insofar as it helps ensure ad-equate perfusionof the head and cerebral vascu-lature at all attitudes of posture (Seymour andLillywhite, 76; Lillywhite, 87). Consider twosnakes which have comparable hydrostatic bloodcolumns above the heart when the body is verti-cal with the head up. Both animals experience anidentical passive drop of pressure at the upperend of the vascular column (due solelyto gravityseffect on hydrostatics) while in the upright pos-ture. However, the snake with the higher arterialpressure has a larger margin of safety beforethe fall in pressure jeopardizes the perfusion he-modynamics at the head, regardless of whether asiphon effect assists the blood flow during up-right posture. Clearly, the heart must develop apressure exceeding that of the hydrostatic columnabove it in order to open the outflow valves andproduce (or maintain) flow (see also Seymour etal., 93).Arterial blood pressure in snakes appearsto be directly related to the distance between theheart and head of terrestrial species (Seymour,87). Indeed, it has been possible to demonstratethat carotid arterial bloodflowbecomes null whenthe arterial pressure measured at heart level de-creasesto avalue just below that required to sup-port the blood column above the heart (Fig. 3).Similarly, data from terrestrial mammals indicatethat levels of systemic arterial pressure exceedthose of the hydrostatic column above the heartwhen the animals are inastanding position. Thus,there is a crude correlation between the charac-teristic arterial blood pressure and heightof largerterrestrial mammals (Patterson et al., 75).In consideration of the above, it appears thatincreasing levelsof arterial pressure are expectedto evolve with some relation to the degreeof gravi-tational stress which a species experiences as aresult of itsheight and postural behavior. Second-arily, other traits which are linked to blood pres-sure must coevolve with the level of arterialpressure. Thus, heart mass scales to the 0.95power in snakes but only 0.77 to 0.91 in otherreptiles which are not as subject to gravitationalstress (Seymour, 87).Increasingly higher systemic pressures createa potential problem in terms of excessive pulmo-nary pressures, inasmuch as the ventricle is singleand the pulmonary and systemic circuits are ana-tomically undivided in noncrocodilian lower ver-tebrates. Therefore, evolution of higher systemic


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220 H.B. LILLYWHITE80-60 -40 -20 -OL

1 m inFig. 3. Simultaneous measurements of carotid arterialblood flow and dorsal aortic pressure measured with refer-ence to heart level in a rat sn,ske,Elaphe obsoleta. The abil-ity of this particular snake to regulate arterial pressure hasbeen compromised by lossof blood volume dueto experimen-tal hemorrhage. The segment cf record illustrates the dynamicresponses to 30" head-up tilt, beginning at the arrow. Notethat carotid blood flow decreases to zero when arterial pres-sureisreducedto alevel (indicated by horizontal dashed line)

where the pressure at the heart equals that of the hydro-static column above the heart. The record indicates that theventricle must produce a pressure in excess of the hydro-static column aboveit in order to produce flow in the ceph-alad direction. Reproduced from Lillywhite and Donald('94),with permission.pressures necessitated the coevolution of somemechanism or suite of factors which maintainsseparation of pressures in the two circuits of theblood circulation. Pulmoinary arterial pressures insnakes are maintained generally below20mm Hgin spite of abroad range of resting systemic pres-sures in various species (Lillywhite and Donald,'94). Presumably, separation of pressures in thetwocircuitsinvolves resistance adjustments in theextrinsic (proximal) pulmonary arteries and (or)functional separation of ejection pressures fromthe ventricle, as in Varcznusspp. (Heisler et al.,'83). Birds and mammstls evolved separation ofsystemic and pulmonary blood flows by means ofan anatomically divided ventricle, so further evo-lution of increased levels of arterial pressure wasnot asproblematic.

CARDI OVASCULARMECHANORECEPTORSAND GROSSANATOMICAL ORGANIZATIONRegulation of arterial pressure involvesanum-ber of interacting control systems in probably all

vertebrates.A prominent control system, and per-haps the most important control of blood pressureduring acute disturbance related to posturechange, isthe baroreceptor reflex. Baroreflexes arepresent in all groups of lower vertebrates, includ-ing fishes (Burggren et al., in press). Their pres-ence in aquatic fishes emphasizes their utility innongravitational contexts and the fact that theirevolution was not associated with factors relatedto gravity stress. The available comparative in-formation indicates that, as in mammals, thereare multiple baroreceptor sites in the central vas-culature of probably most species.The efferent side of the baroreflex activates car-diac activity and the constrictory toneof vascularsmooth muscle. Limited data suggest that effer-ent responses might be more effective in gravity-challenged species (cf. Lillywhite and Pough, '83;Lillywhite and Gallagher, ' 85).However, little in-formation is available to compare the gain ofbaroreflexes in species that are subject to differ-ent degrees of gravitational stress.Baroreceptor sites in snakes occur in associa-tion with arterial outflow tracts adjacent to theheart (Lillywhite and Donald, '94).The heart hasan anterior position in gravity-challenged species(Seymour and Lillywhite, '76; Seymour, '87;Lillywhite, '87), so baroreceptors are positionedwith enhanced capacity to detect changesof pres-sure or vascular distension (Jones and Milsom,'82). In addition to cardiovascular mechanorecep-tors located centrally near the heart, there prob-ably are vascular mechanoreceptors in peripheralvasculature. Clearly it is quite possible that sen-sory inputsto cardiovascular reflexes involve suchperipheral receptors which probably exhibit dif-ferential distributions in variably gravity-sensi-tive species.Other aspects of morphology differ betweenscansorial, gravity-sensitive species and non-scansorial species of snakes. Such characters in-clude, in addition to heart position, length of thevascularized (functional) lung, body length, bodygirth or slenderness, and proportional length ofthe tail (Lillywhite, '87, ' 88) .Thus, there is the expectation that there isevolutionary reorganization of gross anatomi-cal features in species which are subjected to


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GRAVITY ADAPTATION I NLOWER VERTEBRATES 221gravitational stresses related to variation of habi-tat and behavior. Because of their attenuate bodyform, snakes probably reflect this principle inmore exaggerated ways than are apparent in othervertebrate species. Some of the relevant featuresare discussed in further detail below.

THE PROBL EM OF BLOOD POOLING:EVOLUTIONOF AN "ANTIGRAVITY SUIT "The principal problem associated with uprightposture is pooling of blood in dependent vascula-ture and the attendant reduction of venous re-turn to the heart. The problem iswell illustratedby the "orthostatic intolerance" of nonscansorialsnakes, including both aquatic and certain ground-dwelling terrestrial species. When these snakesare tilted to head-up positions, carotid blood flowceases at tilt angles between 30" and 45" (Lilly-

white, '93a). This inability to maintain carotidblood flow during upright posture has been corre-lated with tendencies to blood pooling and ineffec-tual vasomotor control of peripheral vasculature(Lillywhite and Pough,'83;Lillywhite,%a, '93b).How do snakes that have adopted arboreal orclimbing habits avoid the problem of blood pool-ing? Three factors appear to have particular im-portance with respect to this question: these aresize, shape and compliance of the extravascularspace surrounding blood vessels in dependent vas-culature.Size

The majority of scansorial snakes have evolvedwithin three families: Boidae, Colubridae and Vi-peridae. With few exceptions, the arboreal spe-cies tend to be relatively short when comparedwith related members of the same family, manyaveraging less than 1m in length (Lillywhite andHenderson, '93). Arboreal colubrids may be longer,but these species are characterized by a propor-tionately long tail, sometimes comprising morethan40%of the total body length. This latter fea-ture has probable significance for gravitationalhemodynamics because the caudal tissues ofsnakes providea much tighter extravascular en-vironment for blood vessels than does the bodycavity (L illywhite and Henderson, '93).Many arboreal lower vertebrates (such as frogsand lizards) are quite small, and the length of theirvascular columns when upright does not limit thepostural requirements of arboreal habits. Longerspecies (for example varanid lizards) presumablyhave modifications affecting compliance of tissueswhich limit blood pooling,asin snakes.

ShapeArboreal snakes are typically very slender, withratios of circumference-to-length being consider-ably smaller than those of other confamilial spe-cies (Lillywhite and Henderson, '93). The slender

shape is advantageous because a smaller circum-ference provides greater resistanceto agiven dis-tending force than does a larger circumference,reflecting the principle of the Law of Laplace. Evo-lution of an elongated tail allometry mentionedabove also confers the advantage of this principle,irrespective of other selective pressures that mighthave possibly provided the evolutionary drivingforce producing the long tail.Lowcompliance tissues

Scansorial species of snakes exhibit tendenciesto reduced caudal blood pooling during uprightposture. The magnitude of change in tail volumeattributable to the combined pooling of blood andfiltered plasma varies from about 1%n arborealspecies to 9% in aquatic species during head-uptilt in air (Lillywhite, '85a). Such differences inblood pooling might be attributable to morphologi-cal attributes as well as to vasomotor status ofthe resistance and capacitance vessels. The me-chanical properties of snake skin are complex anddepend on factors other than skin thickness orpatterns of scalation (J ayne, '88). Comparativedata from Jayne's study do not allow generaliza-tions about mechanical attributes of the skin ofscansorial species. However, allowing for differ-ences in thickness, skin from a species of arbo-real snake was shown to have greater stiffnessthan that of the nonarboreal species tested, sug-gesting there are differences in the dermal col-lagen fibers or some other feature which remainsto be identified. In spite of variation in mechani-cal properties of integument per se, the compli-ance of subcutaneous compartments depends alsoon how tightly the skin isapplied to the underly-ing tissue. Indeed, the integument of scansorialspecies appears to have tighter and more exten-sive attachment to underlying tissues than doesthat of nonscansorial species (L illywhite andSmits, '92;Lillywhite and Henderson, '93). Thus,compliance of the subcutaneous tissue space wasfound to be greater in aquatic and nonscansorialspecies than in scansorial species of snakes(Lillywhite, '93b). Presumably, such differences ofcompliance reflect adaptive structural modifica-tions related to requirements for counteractinggravitational stresses in the various forms. Fi-


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222 H.B. LILLYWHITEnally, based on whole body volume/pressure rela-tions in vivo, the vasculature in aquatic file snakes(Acrochordus urufurue) s about three times morecompliant than that of terrestrial pythons (Liasisfuscus; Arndt and Seymour,93).These whole bodymeasurements presumably incorporate the stiff-ness of vessels as well as the surrounding bodytissues of the snake.The combined morphological characters whichlimit vascular expansion might be referred to ap-propriately as an anatomical antigravity suit.The importanceof such a feature to gravitationalhemodynamics is illustrated by experimental datafrom a semiaquatic snake (Nerodia rhornbiferu)which was restrained within a tight-fitting tubeduring exposure to graded increases of accelera-tion force produced in the head-to-tail direction(G,) on a centrifuge (Lillywhite et al., 96). Thetight tube prevented expansionof the snakes bodyand thereby increased the level of accelerationwhich the snake could withstand (from+2 to +3G,) without cessationof carotid arterial blood flow.Evidently, this change of response reflects a sub-stantial increase in the cardiovascular tolerancetoG, force due solely to the mechanical countennea-sure, without attendant (changes n physiology.Whether morphological characteristics describedhere for scansorial snakes have evolved in otherlower vertebrates as countermeasures to gravityis not known. However, these features in snakesappear to be convergeint with those of uprightmammals. Giraffes, for example, have very tightskin investing the feet and legs which help tocounteract gravitationaIedema that might other-wise arise from the high levels of blood pressurethat prevail in the dependent limbs of such tallanimals (Hargens et al., 87,88).Aquatic animalsdo not require such features because the surround-ing water column providesapassive, external an-tigravity suit.Thus, natural selection associated with gravi-tational stress favors tightness of externalanatomy and extravascular tissues which therebyprovide an antigravity wit. A summary of thesefeatures in snakes is depicted in Figure4.

BLOODVESSELSP L N D GRADIENTSOFVASCULAR ADAPTATIONThe foregoing discussion brings us to the sub-jectof the blood vessels Ibemselves. Ophidian vas-culature bears adrenergic innervation whichvaries interspecifically in patterns that are corre-lated with the behavior and habitat of species.Ar-boreal and other scansorial species have especially

A

il

B CFig. 4. Comparisons of blood pooling in the circulatorysystems of (A) a generalized arboreal snake, (B) a non-climbing terrestrial snake, and (C) an aquatic snake. Blood

pooling is constrained by morphology and low compliance ofperivascular tissues in the arboreal snake, and by the liquidenvironment external to the aquatic snake. Relatively com-pliant tissues of the nonclimbing terrestrial snake allow con-siderable pooling of blood during hypothetical periods ofupright posture. These examples assume static conditions.Movements and behavior can mitigate pooling in all species,but are more effective in the arboreal forms (cf. L illywhite,85b, 93a). Reproduced from Lillywhite and Henderson (93),with permission.

dense innervationof major arteries and veins pos-terior to the heart, whereas anterior vessels areinnervated more sparsely (Donald and Lillywhite,88, 95).Furthermore, an extensive distributionand colocalizationof neuropeptides in perivascu-lar nerves innervating the larger arteries andveins also indicate there is functional specializationwithin componentsof the peripheral autonomic sys-tem controlling the circulation, especially with re-gard to regulation of venous capacity (Davies andDonald, 92).The patterns suggest there has beenconsiderable adaptive modification in the distribu-tionof perivascular autonomic nervesto the largerblood vesselsof snakes in relation togravitational


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GRAVI TYADAPTATION INdemands that were imposed during their evolu-tionary history.Neurally mediated regulation of vascular resis-tance and capacity is of primary importance incontextsofhomeostatic responses to gravitationalstress (Lillywhite and Seymour, '78). Regionalchanges of blood flow during head-up posture havebeen investigated by means of radiolabeled mi-crosphere distribution in semiarboreal rat snakes(Lillywhite and Gallagher, '85). Blood flow toheart, lung and brain was shownto be regulated,while there was pronounced vasoconstriction andreduced blood flow in splanchnic organs and pos-terior skin and muscle. Thus, cerebral blood flowis maintained by these regional adjustments of flowand resistance, in combination with central shuntsthat redirect flow inacephalad direction (Lillywhiteand Donald, '88) .The major venous pathways lackvalves in many snakes that have been examined(Lillywhite, '871, and the posterior veins of ratsnakes bear anespecially dense innervation (Donaldand Lillywhite, 88).These observations suggest thatneurogenic regulationof venous capacity may be ofparticular importance nscansorial species of snakes(Lillywhite and Donald,'94).Recently the larger blood vessels of rat snakeswere shown to be reactive to vasoactive agonistsin specific anatomic patterns related to the gravi-tational demands of climbing (Conklin et al., '96).In particular, catecholamines stimulate severalfoldgreater tension in posterior than in anterior ves-sels, which were shown to have lesser inherentcontractility in vitro (Fig. 5) . Such data providefunctional correlates of innervation patterns whichmost likely evolved in relation to gravitational in-fluence on postural hemodynamics.Thus, natural selection has produced gradientsor regional differences of vascular characteristicsalong the body length of elongate vertebrateswhich are active in high G-stress environments.Other examples of such regional adaptation in-clude gradients of capillary basement membranethickness which increases twofold from neckmuscle to leg muscleof adult giraffes and humans(Williamson et al., '71). Such membranes in thehuman fetus are uniform and considerably thin-ner than those in children or adults. Regional re-sponses to local differencesof hydrostatic pressurearealsoevident in the variation of medial smoothmuscle (Goetz and Keen, '57; Pettersson et al., '86)and innervation (Nilsson et al., 88 )of giraffe bloodvessels. Similar or novel examples might also beexpected among ectothermic vertebrates but havenot been widely investigated.

LOWER VERTEBRATES 223

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Fig. 5. Maximal tension development of arterial segmentsin relation to anatomical distribution of blood vessels in therat snake,Eluphe obsoleta. Data are shown for mean ( 2S.E.)maximal responses of vascular smooth muscleto norepineph-rine. (Responses to epinephrine and 80 mM potassium areboth qualitatively and quantitatively similar.) Vessel abbre-viations:ADA, anterior dorsal aorta;CA, carotid artery; MDA,midbody dorsal aorta; PDA, posterior dorsal aorta. Data fromConklin et al. ('96).

The condition of structural and functional gra-dients related to gravity adaptation raises someinteresting considerations. For example, there iscurrently great interest in the role of endotheliumin regulating blood flow and resistance in vessels.The question arises, is an endothelial cell an en-dothelial cell, or might endothelial properties varyaccording to regional hemodynamics related togravity? Clearly, the possibility of regional varia-tion in functional propertiesof endothelium shouldbe considered in the planning of experimentsorthe interpretation of data from different speciesof animals. Gravitational factors may well con-tribute to the functional variability that is present.

CONCLUSIONSIn summary, we might expect to find adaptivevariation of form and function in various verte-brates experiencing variable exposure to gravita-tional stresses. Extreme modifications such asthose seen in snakes are related to size, posture,behavioral activities, and terrestriality. Studiesofsnakes indicate that gravity has: (1) nfluencedthe evolution of arterial pressure and its regula-tion; (2) determined, in part, the placement andform of internal organs such as heart and lung;(3) constrained body length in certain environ-ments; (4) ed to modifications of body shape andcompliance of subcutaneous compartments affect-


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224 H.B. LILLYWHITEing blood vessels; (5) influenced structure, com-pliance and functionof blood vessels; and (6)cre-ated gradients or regional variation of structureand function within the body. For gravitationalbiologists who might be interested in applied as-pects of gravity adaptation, such as countermea-sures to space travel, lower vertebrates such assnakes might provide important material for in-vestigations into basic mechanisms and processesrelated to gravitational effects. Whether or notgravitational effects are the focus, studiesof ver-tebrate structure and function should be ap-proached and interpreted with an awareness ofthe generalizations that have been summarizedherein.

ACKN0W:LEDGMENTSWritingof this review, and part of the work onwhich it is based, were undertaken with supportfrom NASA and the National Research Councilwhile the author was a.Resident Associate at theAmes Research Center, Moffett Field, California.

LITERATURE CITEDAmdt, J .O., and R.S. Seymour (1993) Adaptation of the car-diovascular system to gravity: Volume/pressure relations ofthe circulation of terrestrial and aquatic snakes. Abstract90.15P of 32nd I.U.P.S.Congress, Glasgow.Burggren, W.W., A.P. Farrell, and H.B. Lillywhite (1996) Ver-tebrate cardiovascular systems. In: Handbook of Compara-tive Physiology. W. Dantz er, ed. American PhysiologicalSociety, Bethesda, Maryland (in press).Conklin, D.J ., H.B. L illywhite, K.R. Olson, R.E. Ballard, andA.R. Hargens (1996) Blood vessel adaptation to gravity inasemi-arboreal snake.J .Comp. Physiol., B165:518-526.Davies, P.J., and J.A. Donald (1992) The distribution andcolocalization of neuropeptides in perivascular nerves in-nervating the large arteries and veins of the snake,Elapheobsoleta. Cell Tissue Res., 269:495-504.Donald, J.A., and H.B. Lillyv, hite (1988) Adrenergic innerva-tion of the large arteries and veins of the semiarboreal ratsnakeElaphe obsoleta. J .Morph., 198:25-31.Donald, J .A., and H.B. Lillywhite (1995) Adrenergic innerva-tion of the larger arteries and veins of snakes. Faseb J.,9:A354.Gauer, O.H., and H.L. Thron (1965) Postural changes in thecirculation. In: Handbook of Physiology, Sec.2, Circulation,Vol.3.W.F. Hamilton andP. Dow, eds. American Physiologi-cal Society, Washington, D.C., pp. 2409-2439.Goetz, R.H., and E.N. Keen (1957) Some aspects of the car-diovascular system in the giraffe. Angiology, 8:542-564.Hargens, A.R., R.W. Millard, I< Pettersson, and K. J ohansen(1987) Gravitational haemodynamics and oedema preven-tion in the giraffe. Nature, 32959-60.Hargens, A.R., D.H. Gershuni, L.A. Danzig, R.W. Millard, andK . Pettersson (1988) Tissu~sadaptations to gravitationalstress: Newborn versus adult giraffes. Physiologist,31:SllO-S113.Heisler, N., P. Neumann, arid G.M.O. Maloiy (1983) The

mechanism of intracardiac shunting in the lizard Varanusexanthematicus. J . Exp. Biol., 105:15-31.Jayne, B.C. (1988) Mechanical behavior of snake skin. J .Zool.(Lond.), 214:125-140.Jones, D.R., andW.K. Milsom (1982) Peripheral receptors af-fecting breathing and cardiovascular function in non-mam-malian vertebrates. J .Exp. Biol., 100:59-91.Lillywhite, H.B. (1985a) Postural edema and blood poolingin snakes. Physiol. Zool., 58:759-766.Lillywhite, H.B. (198513) Behavioral control of arterial pres-sure in snakes. Physiol. Zool., 58:159-165.Lillywhite, H.B. (1987) Circulatory adaptations of snakes togravity.Am. Zoologist, 27:81-95.Lillywhite, H.B. (1988) Snakes, blood circulation and grav-ity. Sci. American, 256:92-98.Lillywhite, H.B. (1993a) Orthostatic intolerance of viperidsnakes. Physiol. Zool., 66:lOOO-1014.Lillywhite, H.B. (1993b) Subcutaneous compliance andgravitational adaptation in snakes. J . Exp. Zool., 267:

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Journal of Experimental Zoology Part a Ecological Genetics and Physiology Volume 275 Issue 2-3 1996...

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