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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
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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
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| 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. Thus, snakes may provide
valuable models for understanding the
evolution of cardiovascular design as well
as mechanisms of function.
ACKNOWLEDGMENTS
Much of the work on which this article
is based was supported by the National
Institutes of Health research grants HL
24640 and HL 33821. I sincerely thank
Roger Seymour, Warren Burggren and
Allan Smits for reading the manuscript and
offering valuable advice.
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