Download Scaling of Cardiovascular Physiology in Snakes1

AMER. ZOOL., 27:97-109 (1987)
Scaling of Cardiovascular Physiology in Snakes1
ROGER S. SEYMOUR
Department of Zoology, University of Adelaide,
Adelaide 5001, South Australia
SYNOPSIS. The elongate body form of snakes and the wide diversity of habitats into which
they have radiated have affected the form and function of the cardiovascular system.
Heart position is strongly correlated with habitat. The heart is located 15-25% of the
body length from the head in terrestrial and arboreal species, but 25-45% in totally
aquatic species. Semi-aquatic and fossorial species are intermediate. The viperids are
exceptional, with generally more posterior hearts but arboreal species have hearts closer
to the head. An anterior heart is favored when snakes climb because it reduces the
hydrostatic pressure of the blood column above the heart and tends to stabilize cephalic
blood pressure. In water, where hydrostatic blood pressure is not a problem, a more
centrally located heart is favored because the heart does less work perfusing the body. In
terrestrial species, head-heart distance increases linearly with body length and the increased
hydrostatic pressure is matched by higher resting arterial blood pressure in longer animals.
Unlike mammals and birds, snakes have blood pressures that increase with body mass.
The added stress on the ventricle wall in larger snakes is correlated with ventricles that
are larger than predicted by other reptiles. Heart mass scales with body mass to the 0.95
power in snakes but only 0.77-0.91 in other reptiles that are not as subject to the hydrostatic effects of gravity. The spongy hearts of reptiles do not conform well to the Principle
of Laplace.
INTRODUCTION
Vertebrate cardiovascular systems have
evolved in parallel with the metabolic
requirements of the tissues, principally the
demands for adequate gas exchange. Presumably there has been natural selection
for energetic economy in the system. Optimally, the blood should be moved with the
least work while the animal's metabolism
remains aerobic during routine behavior,
but enough reserve capacity should exist
to meet vital requirements imposed by
environmental exigencies. However, the
characteristics of the system may not be
energetically optimal because they are constrained by many environmental, morphological and behavioral factors.
The work done by the heart is approximately proportional to the product of the
blood flow rate (cardiac output) and the
mean blood pressure. Blood flow rate is
related to the metabolic rate which, in turn,
is related to body mass. Blood pressure has
two components, namely, a hemodynamic
component that depends on the resistance
to blood flow in the vessels and a hydrostatic
1
From the Symposium on Cardiovascular Adaptation
in Reptiles presented at the Annual Meeting of the
American Society of Zoologists, 27-30 December
1984, at Denver, Colorado.
97
component that depends on the absolute
vertical distance that blood is pumped
above the heart. Thus blood pressure
depends somewhat on body size. Larger
animals tend to have higher hydrostatic
components of blood pressure, and the
heart may do more work raising the blood
column above it. The hydrostatic component is important only in land animals. In
aquatic species, the hydrostatic pressure of
the external water column almost completely compensates for the blood column.
An important correlate to blood pressure is heart mass. Vertebrate cardiac muscle operates within a limited range of stress
and adaptively compensates for increased
load by increasing its mass (Goss, 1971).
The adaptation may be physiological or
phylogenetic. Physiologically, when the
arterial blood pressure changes {e.g., during training in athletes or after exposure
to high altitude), the walls of the heart
hypertrophy or atrophy, tending to compensate for the load. Phylogenetically,
there are many demonstrations of the relationship between cardiac mass and stress
on the ventricular wall. In general, hearts
are relatively larger in similarly sized animals with higher metabolic rates or higher
arterial blood pressures {e.g., Goetz and
Keen, 1957; Hudson and Brush, 1964;
98
ROGER S. SEYMOUR
Poupa and Ostadal, 1969; Poupa and Lindstrom, 1983).
Of course, heart mass increases with body
mass in animals. Exactly how it increases is
the subject of allometric analyses that have
now been performed on a variety of vertebrates {e.g., Hesse, 1921; Clark, 1927;
Hartman, 1955; Brush, 1966;Stahl, 1967;
Poupa and Ostadal, 1969; Lasiewski and
Calder, 1971; Prothero, 1979; Poupa and
Lindstrom, 1983). However, uniform data
from reptiles are scarce (Else and Hulbert,
1983; Poupa and Lindstrom, 1983; Garland, 1984).
Among the reptiles, the snakes are of
prime interest with respect to the effects
of morphology, environment and behavior
on the cardiovascular system. They have a
wide variation of body size and length and
they live in an extreme diversity of gravitational environments, ranging from totally
aquatic to totally arboreal. Seymour and
Lillywhite (1976) discovered adaptive
trends in blood pressure regulation and
heart location in nine species of snakes from
different habitats. The present report
extends the data base and examines heart
mass, heart position and blood pressure in
relation to body mass, length of" the major
arteries, and the effects of gravity.
Boiga, Dendrelaphis, Chondropython). (5) Ter-
restrial species cannot be classified easily
into the above groups {e.g., most elapids
and pythons). The terrestrial group is the
largest and includes not only the indisputably terrestrial snakes that are found away
from water or trees, but also some species
occasionally found swimming or climbing
vertically. Most non-aquatic snakes are able
to swim and climb with apparent ease and
may feed to a significant extent on aquatic
or arboreal prey. However, they are most
often found on the ground. At least for the
present discussion dealing with the effects
of gravity on hemodynamics, all snakes
without specialized morphology or behavior for arboreal or aquatic life seem better
allied with the generalized terrestrial
species. (6) Viparid species are separated
from the rest a posteriori because they are
exceptional as discussed below.
Blood pressure values were collected
from 29 individuals of 13 species of Australian snakes as they became available
between 1975 and 1981. The animals were
measured within a month of capture and
with body temperatures of 25 ± 2°C. Temperature differences within this range do
not affect blood pressure (Lillywhite and
Seymour, 1978). During cold anaesthesia,
the aorta was occlusively catheterized at a
METHODS
level just anterior to the cloaca. The cathBody mass, body length and heart posi- eter was fashioned from polyethylene tubtion were measured in 412 snakes of 95 ing of appropriate size and was filled with
species. Most specimens were fresh but heparinized (250 i.u./ml) saline. After a
some were preserved intact in the South recovery period of at least 24 hr in isolaAustralian Museum. The snakes were clas- tion, mean blood pressure was measured
sified in six categories according to per- in undisturbed animals as they rested in
sonal knowledge or descriptions of the pri- their holding boxes. While avoiding all
mary behavior in Cogger (1983), Wright visual and most acoustic interference from
and Wright (1957) and Ditmars (1946). (1) the investigator, the catheter was conFossorial species primarily burrow in the nected to a Statham P23AC strain gauge
ground or litter {e.g., Typhlina, Vermicella). transducer and a Grass model 7D oscillo{2) Aquatic species rarely come on land, pos- graph, previously calibrated against a water
sess obvious morphological adaptations for manometer. Mechanical and electrical
swimming, and are viviparous {e.g., hydro- damping resulted in mean blood pressure,
phiid sea snakes, acrochordids). (3) Semi- measured at heart level. The small kinetic
aquatic species are commonly found in energy of blood is ignored and it was
water where they feed but often rest on assumed that there was no pressure drop
shore, for example to bask or lay eggs {e.g., between the heart and the site of catheterhomalopsines, laticaudid sea snakes). (4) ization. Blood pressures in these circumArboreal species are often long and slender stances were usually a little lower than those
snakes most commonly found in trees {e.g., obtained from the same animals in
99
SCALING SNAKES
TABLE 1. Multiple comparisons among means of relative
heart position (7c body length) in six groups of snakes (analysis of variance and Student-Newman-Keuls test).
Aquatic
Viperid
Ar- Terrcs- SemiFosboreal trial aquatic sorial Viperid Aquatic
Mean
SD
Arboreal
Terrestrial
Semiaquatic
Fossorial
Viperid
Aquatic
o 30
9
2 20
17.4
2.2
18.8 22.7 23.6 33.3 33.4
3.2
7.9 4.5 5.7
4.8
*
NS
*
*
NS
—
NS
* Significant (P < 0.05).
10 g
100 g
Body Mass
Ikg
10 kg
FIG. 1. Heart position as a percentage of body length
from the head in snakes. Each point represents a species
mean and the species are grouped according to criteria described in the text. The outlined areas enclose
the data from six groups: totally aquatic (open squares),
viperid (filled squares), semi-aquatic (open circles),
terrestrial (filled circles), arboreal (open triangles) and
fossorial (filled triangles).
restraining tubes during tilting experiments. Heart rate was determined from
some of the blood pressure records by
averaging the rate over several breathing
cycles.
Specimens of the Australian black snake,
Pseudechis porphyriacus, were subjected to
tilting experiments as described earlier
(Seymour and Lillywhite, 1976; Lillywhite
and Seymour, 1978).
After experimentation, the snakes were
killed with anaesthetic injected through the
catheter. They were weighed and the distances measured between the head (eye),
heart and tip of tail. The heart was
removed, the atria and vessels carefully cut
free, the blood was squeezed and blotted
away, and the ventricle weighed. Heart
mass was available from 101 fresh specimens of 29 species. The hearts were fixed
in formalin, embedded in wax, stored and
later sectioned and stained with Weigert's
iron haemotoxylin and Van Gieson's stain.
With a microscope fitted with a drawing
tube, the cross section of each heart was
traced at a point equidistant from the apex
and base. The outer circumference and the
wall thickness in four places were then
measured from the enlargements with a
rotary distance gauge and ruler.
RESULTS
Heart position
There is a clear relationship between
heart position and habitat in most species
(Fig. 1; Appendix). Analysis of variance and
the Student-Newman-Keuls a posteriori test
of sample means (Sokal and Rohlf, 1969)
show that the following pairs are not significantly different: (1) arboreal and terrestrial, (2) semi-aquatic and fossorial, and
(3) aquatic and viperid (Table 1). All other
comparisons are significant at P < 0.05.
Arcsin transformation of heart position
does not alter significance of differences.
The hearts of aquatic species are significantly farther toward the body center than
those of the arboreal-terrestrial groups and
the semiaquatic-fossorial groups are statistically intermediate. The viperids are
exceptional because they are terrestrial or
arboreal in habitat yet some species have
hearts in the same location as do aquatic
species. However, since this paper was sent
to press, heart position was found to be
20% in Lachesis muta and 27% in Bothrops
atrox. The South American arboreal viperids are not included in Figure 1. The present data are consistent with data of
Thompson (1913, 1914).
There is no significant correlation
between relative heart position and log
body mass except in the fossorial species
(Fig. 1). Overall, the heart never appears
closer to the head than about 15% of the
body length nor farther back than 45%.
Relative heart position is also independent of total body length as shown by the
linear relationship between absolute head-
100
ROGER S. SEYMOUR
y lOOmg
10kg
100
ISO
Total Length (cm)
FIG. 2. Absolute distance between head (eye) and
heart as a function of body length in six groups of
snakes. Each point represents a species mean (see Fig.
1 for symbols). Regression lines are included for
aquatic and terrestrial species.
heart distance and total length (Fig. 2).
Absolute head-heart distance increases linearly in longer snakes within the groups;
there is no tendency for reduced head-heart
distance in longer snakes. Analysis of
covariance shows that the slopes of the
regressions for the six groups are different
(P < 0.001).
Ventricle mass
In 29 species of snakes, ventricle mass
(Mv, in g) increases with body mass (Mb,
in kg) according to the relation, Mv =
1.64 Mb0934, within the body mass range of
1.5 g-4.4 kg (Fig. 3; Table 2). Although
the aquatic and viperid species tend to have
smaller hearts, there are no significant correlations with habitat groups (see Appendix). Poupa and Lindstrom (1983) provide
values of total heart mass (Mh) infivespecies
FIG. 3. Ventricle mass as a function of body mass in
snakes. The points represent 101 individuals of 29
species. The axes are logarithmic and the regression
of the data is the solid line. The dashed line represents
unplotted data of total heart mass in 10 individuals
of 5 species of snakes from Poupa and Lindstrom
(1983). The equations and statistics for these lines are
in Table 2.
of snakes with a body mass range of 0.34
g-19.5 kg. The regression equation based
on their data (Mh = 2.9lM b 0986 ) is significantly above the present equation because
they included the atria, but the slope is not
significantly different from the present
value (ANCOVA: elevation, F = 20.6,
d.f. = 1,108; slope, F = 2.64, d.f. = 1,107).
The common slope of the two data sets
(0.947) is significantly less than 0.99 and
more than 0.91 (P < 0.05).
Unfortunately the hearts in the present
study were stored for too long in wax and
the spongy tissue often broke away when
sections were cut. However, the outer compact layer remained intact in most specimens. Assuming that the ventricle was a
TABLE 2. Allometnc equations for ventricle mass (MJ, heart mass (MJ, mean arterial blood pressure (B.P.) and heart
rate (H.R.) in snakes.*
Y
X
a
b
M,(g)
Mh(g)
Mb (kg)
Mb (kg)
1.64
2.91
0.934
0.986
B.P. (kPa)
B.P. (kPa)
B.P. (kPa)
H.R. (beats/min)
Mb (kg) 5.25
Mb (kg) 5.80
5.11
M.(g)
Mb (kg) 20.6
0.154
0.227
0.248
-0.229
*\x
SE,
r
0.018 0.017
0.016 0.027
0.98
0.99
0.050
0.063
0.080
0.083
0.51
0.68
0.64
-0.64
0.022
0.025
0.027
0.037
n
56
37
3.07
3.59
3.11
-2.76
101
10
29
17
16
13
Group
All
All, Poupa and
Lindstrom, 1983
All
Terrestrial
Terrestrial
Terrestrial
* The form of the equation is Y = aXi. The statistics are unexplained mean square (s!Y.x). standard error
of the slope (SEt), correlation coefficient (r), the ( statistic for expected 6 = 0, and number of animals (n).
101
SCALING SNAKES
1
FIG. 4. Mean arterial blood pressure in resting snakes
from different habitats. The points represent 29 individuals of 13 species (see Fig. 1 for symbols). The axes
are logarithmic and the regression of the data representing only the terrestrial species (dots) is shown
with the 95% confidence belt of the regression (equation and statistics in Table 2).
sphere, the volume of the compact layer
could be roughly estimated from its circumference and the thickness. This volume averaged 24.7% of the entire volume
of the intact fresh ventricles determined
from mass.
Blood pressure
Mean resting arterial blood pressure (BP,
in kPa) is significantly correlated with body
mass (Mb, in kg) in terrestrial snakes (Fig.
4). The equation for the relation is: BP =
5.80Mb0227, within the body mass range of
0.028-4.0 kg (Table 2). With data from all
available snakes, there is still a significant
correlation, but the equation becomes BP =
5.25Mb0154 (Table 2). The reduced exponent results from blood pressure tending
to be higher in arboreal species and lower
in aquatic species, compared to terrestrial
species (Seymour and Lilly white, 1976), and
the arboreal species being small and the
aquatic species being large (Fig. 4).
Because ventricle mass is related strongly
to body mass, it is not surprising that arterial blood pressure is also significantly
related to ventricle mass. The regression
equation is BP = 5.11MV0248, where BP is
in kPa and Mv is in grams (Table 2). Similarly, blood pressure is significantly related
to body length (Lb, in cm) in terrestrial
2
3
4
5
6
Head-Heart Hydrostatic Pressure (kPa)
FIG. 5. Mean arterial blood pressure in 16 individuals of 9 species of terrestrial snakes related to the
hydrostatic pressure of a vertical blood column equivalent to the distance between the heart and head.
Blood was assumed to have a density of 1.05 g/ml.
The least squares regression equation is y = 1.18x +
2.26 (SE4 = 0.40, r = 0.62, t = 2.95). The dashed
curves define the 95% confidence belt of the regression and the lowest line has a slope of 1.0.
snakes according to the linear equation
B P = 0.0269L b + 1.843 (r = 0.561, n =
17, t — 2.62) and in all snakes according to
the equation BP = 0.0238Lb + 1.991 (r =
0.517, n = 28, t = 3.08).
Blood pressure appears to be directly
related to the distance between the heart
and head of terrestrial species. When the
distance is converted into a hydrostatic
pressure of a vertical blood column, the
relationship has a slope of 1.18 which is
not significantly different from 1.0 (Fig. 5).
Heart rate in resting terrestrial snakes
at 25°C is inversely related to body
mass according to the equation: HR =
20.6Mb~0229, where heart rate is in beats/
min and Mb is in kg (Fig. 6; Table 2). The
exponent of this equation is more extreme
than the value (—0.155) found in varanid
lizards at 30°C (Bartholomew and Tucker,
1964), but the two exponents cannot be
statistically distinguished because of high
variability in the data.
Black snakes, Pseudechis porphyriacus,
showed responses qualitatively similar to
those of other terrestrial snakes subjected
to tilting (Seymour and Lillywhite, 1976;
Lillywhite and Seymour, 1978). Immedi-
102
20g
ROGER S. SEYMOUR
50g
500g
Body Mass
FIG. 6. Mean heart rate in 13 individuals of 9 species
of resting terrestrial snakes at 25°C. Both axes are
logarithmic and the regression line is shown with the
95% confidence belt (equation and statistics in Table
2).
ately after head-up tilting, there was a transient drop in blood pressure measured at
the body center. This was followed by
physiological responses that increased central blood pressure. Figure 7 shows values
from tilted snakes after these initial passive
changes and active responses had stabilized. During head-up tilting, the snakes
showed a pattern of regulation similar to
other terrestrial species (Seymour and Lillywhite, 1976). Blood pressure at the body
center increased sharply with tilt angle.
Head-down tilting revealed little regulation as central blood pressure remained
fairly constant.
DISCUSSION
Heart position
In some contexts, the word "heart"
means the central part, and, in most vertebrates, the heart is quite near the center
of the body mass. In most terrestrial and
arboreal snakes, however, the heart is only
15-25% of the total body length away from
the head (Fig. 1). An advantage of this
anterior position appears when the snake
raises its head. The vertical distance
between the heart and the brain, and hence
the hydrostatic pressure of the blood column, are minimized and passive blood
pressure changes in the brain are reduced.
Although many reptiles can tolerate high
60
40
20
Head Down
T.I! Angle (")
FIG. 7. Stabilized arterial blood pressure at the body
center of five black snakes, Pseudechis porphynacus,
during passive head-up and head-down tilting.
levels of anaerobiosis, it appears important
for them to maintain cephalic blood flow
because they quickly die if blood flow to
the brain is stopped (Belkin, 1968).
The effect of heart position on cephalic
blood pressure may be illustrated by passive tilting experiments. Figure 8 shows the
effects of passive head-up tilting on blood
pressure in the brain of the black snake,
Pseudechis porphyriacus. In this snake, the
heart position averages 19% of the body
length. Also shown are two curves representing the calculated brain blood pressure
that would occur if the pressure at the heart
remained constant at 3.86 kPa. One curve
has the heart in the normal position (19%
of body length) and the other is the hypothetical midbody position (50% of body
length). The differences between the actual
data and each of the calculated curves represent the increase in blood pressure (hence
the increase in work) that must be produced by the heart to maintain brain blood
pressure as constant as it is. Were the heart
located in the center of the body, considerably more work would be required to
keep cephalic blood pressure from dropping.
if maintenance of brain blood pressure
is important, there should be selection for
a heart position near the head in species
that climb, especially if the site of baroreception lies somewhere near the heart.
103
SCALING SNAKES
25
0
10
20
30
40
50
60
70
80
90
Tilt Angle (")
Heart
50
Position
75
100
(% body length)
FIG. 8. Cephalic blood pressure in the black snake,
Pseudechis porphyriacus, during passive head-up tilting.
Values are mean ± SE; n = 5. The dashed lines are
calculated cephalic pressures based on the assumption
that pressure at the heart remains constant during
tilting and that the heart is at the actual site (19% of
the body length from the head) or at a hypothetical
mid-body site (50%).
FIG. 9. Arterial blood pressure at the heart as a function of heart position in a hypothetical snake consisting of a series of identical segments. The model is
based on a 300 g animal with a systemic cardiac output
of 18 ml/min, a distal minimum blood pressure of 4
kPa, and arterial blood volumes of 0.25, 0.5, 1.0 and
2.0 ml in a single vessel (carotid plus aorta) running
the length of the 1 m body. The estimated volume of
these major arteries in a real snake is between 0.5
and 1.0 ml, based on unpublished data.
Baroreceptive activity in the lizard, Trachydosaurus rugosus, occurs close to the heart,
probably in the tuncus arteriosus and is
absent from the carotid region (Berger et
ai, 1980). The pulmonary artery is implicated in turtles (Faraci et ai, 1982). Among
snakes, blood pressures at heart level
remain fairly constant during head-up tilting in terrestrial and arboreal species, but
not in aquatic and semiaquatic species (Seymour and Lillywhite, 1976; Lillywhite and
Seymour, 1978). Cephalic blood pressure
always falls significantly during tilting.
Because only slight changes in blood pressure should occur at the functional site of
baroreception, some baroreceptive activity
appears anterior to the heart. In fact, an
external cuff technique has shown that the
entire region between the heart and the
head, possibly along the length of the
carotid artery, is involved in two species of
terrestrial snakes, Bothrochilus fuscus and
Pseudechis porphyriacus (Seymour and
Barker, 1983). This evidence supports the
hypothesis that elongation of the body of
some terrestrial snakes has selected for
anterior heart position and involvement of
the carotid area in baroreception, both
adaptations tending to stabilize cephalic
blood pressure.
Despite the advantages in keeping the
heart close to the head, there are hemodynamic disadvantages. One problem is
that the pressure in the venous side of the
circulation is also subject to effects of gravity and it may be difficult for blood in the
venous system to return to an anteriorly
placed heart in climbing snakes (Lillywhite, 1987). Venous pooling in the body
below the heart reduces cardiac output and
causes central arterial blood pressure to
drop. This effect can have catastrophic
results in some snakes, especially aquatic
species with poor baroregulation in which
venous return may drop to zero during tilting (Seymour and Lillywhite, 1976; Lillywhite and Pough, 1983).
Another disadvantage is that the farther
the heart is away from the body center, the
more unequal are the amounts of blood
pumped to the anterior and posterior parts
of the body. This imbalance may result in
104
ROGER S. SEYMOUR
a greater workload for the heart. To
appreciate this effect, consider a theoretical snake consisting of identical segments
which are perfused in parallel from
branches of two large arteries, e.g., the single carotid artery and the aorta (Fig. 9). If
the heart produces pressure, Ph, and there
exists a minimum pressure required to perfuse the distal tissues, Po, then the pressure
drop from the heart to the most distal segments is (Ph — Po). Assuming (1) that this
pressure drop is linear from the heart to
the head and tail and (2) that the rate of
blood flow past a particular segment is proportional to the sum of the number of more
distal segments, one can calculate Ph
according to a model derived from the
Poisuille equation. The model is:
respond to changing demands, and less
oxygen is consumed by the blood on its way
to tissue. Second, the work done by vascular smooth muscle may be reduced in
smaller vessels because wall tension is
inversely related to radius according to the
Principle of Laplace. Third, thinner arteries take up less space, which is important
in the body design of snakes, and reduce
by a minor degree the total volume of blood
required to be maintained.
Of course it is presently impossible to
equate all of the advantages and disadvantages of heart position and arterial vascular
dimensions. Nevertheless, it is clear that in
the zero gravity environment of aquatic
snakes, there is little advantage in having
the heart close to the head and we see a
more central placement in these species
(Fig. 1). At the other extreme, the terrestrial and arboreal species are most subject
° \X(Vlot)2
to the effects of gravity and have hearts
closest to the head. Interestingly, there is
no tendency to reduce head-heart distance
in longer terrestrial or arboreal species.
The increased hydrostatic pressures of
longer arterial blood columns in larger
Vx + i - N
snakes is completely offset by higher artewhere X is the total number of segments, rial blood pressure (Fig. 5).
N is the segment number, H is the segment
The patterns in heart position we see
containing the heart, Qtot is the total car- today probably represent evolutionary
diac output into the two vessels, and Vtol is convergence. The totally aquatic hydrothe total blood volume of the two vessels. phiid sea snakes and the semi-aquatic latiHolding Vtot constant and moving the heart caudid sea snakes appear to be two indealong the length of the snake, Ph is shown pendent lines of descent from an elapid
to be minimal at the body center (Fig. 9). stock (McDowell, 1969). Similarly, the
A centrally located heart therefore does acrochordids and homalopsines presumless work in perfusing the body. (Ph — Po) ably evolved independently from colubrid
increases about 4-fold as the heart is moved ancestors (McDowell, 1979). Heart posifrom the center of the body to the end.
tion in the ancestral snakes cannot be
It is also apparent from Figure 9 that the known for certain, but there is some evivolume of the arteries is an important dence favoring a more posteriorly placed
determinant of P h . The work of the heart heart. Snakes in general are thought to
decreases if the arteries increase in radius have evolved from platynotan lizards and
and volume. Small differences in radius can may have been primitively fossorial
have great effects on Ph because the pres- (McFarland et al., 1979). Platynotans
sure drop along a tube is inversely pro- include recent varanids that are characterportional to the radius to the fourth power. ized by relatively long necks and a heart
However, there are also advantages in min- farther back in the body cavity than in other
imizing arterial blood volume. First, a lower lizards (Seymour, unpublished). The earvolume means that the blood travels from less monitor, Lanthanotus, a platynotan with
the heart to the periphery more rapidly. strong aquatic tendencies (Sprackland,
Thus the cardiovascular system can quickly 1972), is thought to be the living lizard
SCALING SNAKES
most similar to the ancestors of snakes
(McFarland et al., 1979). Thus a more centrally located heart may have been associated with fossorial or semi-aquatic behavior in primitive snakes as it is in snakes
today (Table 1).
It is interesting that heart position in
some viperids runs contrary to the clear
relationships shown by most snakes in this
stud. Viperids are generally terrestrial yet
have hearts as far back in the body as most
totally aquatic species (Fig. 1). Viperids are
also similar to totally aquatic species by
having a tracheal lung, which is an extensive, well-vascularized portion of the lung
that runs along the course of the trachea
anterior to the heart (Kardong, 1972;
Heatwole and Seymour, 1975). Among the
advantages of the tracheal lung are that it
adds buoyancy to the anterior part of
aquatic snakes and helps them raise the
head to breathe. It also reduces the dead
space in the trachea which otherwise would
be considerable in the snakes with posteriorly placed hearts, and it permits ventilation while a large food object in the stomach presses against the lung.
There may have been less selection for
anterior heart placement in terrestrial
viperids because they are generally short
and bulky snakes that are usually horizontal. Among crotalines, there is a tendency
for the shorter species to occur in mountainous regions and the longer species to
occur on the plain (Wright and Wright,
1957). This distribution may relate to the
climbing ability. The arboreal Bothrops
schlegeli is a relatively short snake but other
Bothrops and Lachesis species can approach
2 m in length (Ditmars, 1946). Although
the larger specimens appear less likely to
climb (March, 1928; Test et al, 1966; Henderson et al., 1976), the hearts in these
South American species are closer to the
head than in their North American relatives.
Scaling of ventricle mass:
Compact vs. spongy hearts
A useful frame of reference for evaluation of snake hearts comes from the work
on vertebrate endotherms. In general,
heart mass in endotherms approximately
105
scales with body mass to the power of 1.0;
that is, the hearts of different sized animals
within a particular group are a constant
fraction of the body mass (Hesse, 1921;
Clark, 1927; Hartman, 1955; Brush, 1966;
Stahl, 1967; Holt et al., 1968; Poupa and
Ostadal, 1969; Lasiewski and Calder, 1971;
Prothero, 1979; Grubb, 1983; Poupa and
Lindstrom, 1983). Stroke volume also scales
to the 1.0 power and arterial blood pressure is said to be independent of body mass
in mammals and birds (Stahl, 1967; Holt
et al., 1968; Grubb, 1983). Therefore, the
stroke work, which is the product of stroke
volume and arterial blood pressure, scales
with mass to the 1.0 power. The rate of
heart work is the product of the stroke
work and the heart rate, which scales to
the —0.25 power in endotherms. Allometrically, this relation is: Mb075 = Mb'-°Mb~0-25. Thus heart work rate scales to the
same power as metabolic rate, and it
becomes apparent that heart mass is not
proportional to heart work rate, but
increases more quickly than work rate with
increasing body mass.
The scaling exponent for heart mass is
explicable according to the Principle of
Laplace. At least in mammals, the mass of
the ventricular wall is nearly a constant
fraction of the body mass and, because
arterial blood pressure at the beginning of
systole is the same in hearts of all sizes,
stress on the myocardial tissue is more or
less constant (Martin and Haines, 1970).
Thus larger hearts are thicker.
Although the Principle of Laplace is valid
for ventricles that are hollow and have
compact walls as in endotherms, it loses
some validity in many ectothermic vertebrates because their hearts consist of a substantial proportion of spongy tissue beneath
the compact layer of the wall (Johansen,
1965). The mean volume of the compact
layer represents only 25% of the total ventricular muscle volume in snakes of this
study. The blood in the lacunae of the
spongy tissue may be thought of as being
pumped by many small hearts in parallel.
The spongy layer therefore becomes independent of the Principle of Laplace so the
volume of the entire heart should scale with
body mass to a power somewhat less than
106
ROGER S. SEYMOUR
1.0. In fact, the mass of spongy hearts in
ectotherms has an allometric exponent of
0.743 (Poupa and Ostadal, 1969). Individual studies on non-snake reptiles also show
low exponents: Else and Hulbert (1983)
provide the equation, Mh = 2.25Mb°77 (Mb =
0.02-3 kg), for lizards, turtles and crocodiles combined; Garland (1984) gives Mh =
2.16Mb091 (Mb = 0.012-0.87 kg) for the
lizard, Ctenosaura similis and calculates Mh =
2.89Mb0-82 (Mb = 0.131-99 kg) for Alligator
mississippiensis based on data of Coulson and
Hernandez (1983). However, the two studies of snakes show significantly higher allometric exponents (0.93, present study; 0.99,
Poupa and Lindstrom, 1983) than the values from other reptiles. This result could
be due to the positive exponent of blood
pressure in snakes. The data from other
reptiles come from animals that are relatively small or compact (lizards, turtles) or
do not raise the head much above the heart
(crocodilians). Therefore these reptiles
cannot develop high head-heart hydrostatic pressure. As snakes become longer,
however, they become increasingly subject
to hydrostatic pressure loads on the heart
and this is reflected in elevated values of
blood pressure and heart mass.
CONCLUSIONS
The form and function of the cardiovascular system of snakes appear to have
been influenced by the gravitational environments into which snakes have radiated.
Aquatic species, in a zero gravity environment, tend to have centrally located hearts
which are energetically more efficient in
that location. Terrestrial and arboreal
species, at the other extreme, tend to have
hearts located closer to the head, presumably to help stabilize cephalic blood pressure when the head is raised. Blood pressure increases with body length in
terrestrial snakes and offsets the potentially higher hydrostatic pressure of the
blood column between the heart and the
head. The scaling exponent for ventricle
mass, in turn, reflects blood pressure and
is higher in snakes than in other reptiles.
It should be recognized that these conclusions indicate adaptive trends based on
a sample size that represents only \% of
the snake species of the world. The vipers
already emerge as one exceptional group
and it would not be surprising to find others with attributes modified by factors
besides gravity and body size. There
remains great potential for further work
on blood pressure and its regulation in
snakes, especially if the phylogenetic component of variability could be reduced.
Particularly useful in the present context
would be a study of the ontogenetic changes
in cardiovascular morphology and physiology in relation to behavior and growth
in a single large species.
ACKNOWLEDGMENTS
I greatly appreciate the comments on the
manuscript by Harvey Lillywhite, Harvey
Pough and David Bradford. The data on
American species were generously provided by Harvey Lillywhite. The data on
sea snakes were obtained by the author on
an expedition of the R. V. Alpha Helix,
organized by William Dunson. The
remainder of the snake research was supported by the Australian Research Grants
Scheme. Susan Barker, Sandra Powell and
Helen Vanderwoude assisted with data collection and histological work and David
Bradford helped with statistical analysis.
Ted Garland and Henry John-Alder kindly
provided unpublished information. The
figures were drawn by Ruth Altmann and
the text typed by Heather Kimber.
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108
ROGER S. SEYMOUR
APPENDIX. Data on heart position and ventricular mass in snakes. The data indicate the mean body mass (Mb), mean
body length (Lb), mean and SD of heart position (% Lbfrom head) with number of fresh and preserved animals (n F/P),
and mean and SD of ventricle mass (Ma as % Mb).
(g)
(cm)
Heart position
« U)
Mean
SD
» (F/P)
37
43
23
30
26
38
42
31
34
29
36
33
28
28
2
2
0.6
10/4
10/0
14
25
24
29
20
31
21
20
15
19
2
2
0.8
2
2
2
0.5
1
20
18
19
23
22
16
23
23
24
17
20
15
26
14
16
15
16
16
25
18
18
19
23
16
15
17
25
15
16
2
1
M. (% Mb)
Mean
SD
n
0.147
0.193
0.022
0.033
9
2
0.363
0.08
7
Aquatic species
Acrochordus arafurae
Acrochordus granulatus
Aipysurus eydouxii
Astrotia stokesii
Hydrelaps darwiruensis
Hydrophis belcheri
Hydrophis cyanocinctus
Hydrophis elegans
Hydrophis gracilis
Hydrophis inornatus
Hydrophis major
Hydrophis ornatus
Lapemis hardwickh
Pelamis platurus
1,298
100
52
22.4
260
39.3
2,450
107
258
156
330
30
131
60.8
73.3
47
39.1
85.2
56.8
198
45.5
61.4
91
64.5
63.5
63.7
3
2
3
2
2
2
9
0/2
1/0
0/4
8/0
6/0
1/0
0/1
5/0
0/1
29/0
4/0
1/2
Semi-aquatic species
Amphiesma mairii
Cerberus australis
Cerberus rhynchops
Enhydris polylepis
Fordonia leucobalia
Laticauda colubrina
Laticauda laticaudata
Laticauda semifasciata
Nerodia sipedon
Nerodia taxispilota
36.8
105
132
154
515
165
641
240
228
48.9
50.0
64.2
66.4
54.5
115
88.3
102
101
79.8
0.5
0/4
0/3
9/2
0/4
0/5
23/0
6/0
16/0
1/0
3/0
0.14
1
0/2
1/0
1/4
0/3
0.153
0.189
1
1
4/11
0.13
0.031
2
0.15
0.148
0.023
8
1
0.182
0.011
2
0.208
0.028
6
0.169
0.022
9
0.218
0.02
2
0.179
0.18
0.039
1
4
0.201
0.057
4
Terrestrial species
Acanthophis antarcticus
Acanthophis pyrrhus
Arizona elegans
Aspidites melanocephalus
Aspidites ramsayi
Auslrelaps superba
Bothrochilus childreni
Bothrochilus fuscus
Bothrochilus olivaceus
Brachyaspis curta
Brachysoma christeanus
Cacophis squamulosus
Candoia cannata
Coluber constrictor
Cryptophis nigrescens
Demansia olivacea
Denisonia devisi
Diadophis punctalus
Echis carinatus
Elaphe obsoleta
Elaphe radiata
Furina diadema
Clyphodon trtstis
Hemiaspis signata
Lampropeltis getulus
Masticophis piceus
Morelia spilota
Notechis ater
Sotechis scutatus
252
148
161
1,362
3,900
339
339
953
3,305
6.5
45.7
530
182
35
56.7
58.5
107
131
195
55.3
76.9
149
240
42.5
35.8
72.6
78
116
48.1
122
4.48
30.2
510
50.5
15
147
35.8
258
475
1,533
505
226
36.8
24.9
44.5
138
74
38.8
86
52.9
112
181
137
105
87
0.8
2
1
2
0.6
0.7
3
2
0.1
1
2
2
1
0.7
0
0.7
1
4
0
1
0/11
0/5
4/0
1/0
0/3
0/1
2/0
0/2
2/0
0/4
0/1
0/3
6/0
0/1
17/0
0/1
0/4
0/2
2/0
1/0
2/0
4/5
1/3
4/6
109
SCALING SNAKES
APPENDIX.
Mb
(g)
Oxyuranus scutellatus
Parademansia microlepidota
Pituophis melanoleucus
Pseu4echis australis
Pseudechis porphyriacus
Pseudonaja ajfinis
Pseudonaja nuchalis
Pseudonaja texlilis
Rhinoplocephalus bicolor
Suta suta
Tropidechis cannatus
Unechis flagellum
753
838
747
642
304
368
464
469
17.4
Continued.
u
(cm)
210
166
162
144
76.6
107
138
136
34
40
Heart position
(» U)
Mean
SD
n (F/P)
20
17
19
18
19
17
18
17
18
20
16
19
1
0.3
0/3
0/3
1/0
0/3
3/5
0/5
0/5
2/5
0/2
1/0
1/3
2/0
170
7.05
82.1
25.6
48
9.25
43.3
11.5
32.8
25.6
35
51
31
17
15
19
19
0.2
2
1
0.8
1
2
1
0
M. (X MJ
Mean
SD
n
I
0.119
0.283
0.077
11
0.202
0.008
2
0.19
0.238
0.008
2
1
Fossorial species
Ramphotyphlops australis
Ramphotyphlops bituberculatus
Ramphotyphlops polygrammicus
Simoselaps incinctus
Simoselaps littoralis
Vermtcella annulata
Vermicella fasciolata
7.75
14.5
9.5
27.8
21.5
48.2
29.1
29
0.7
1
1
2
0.9
0/2
0/2
0/2
0/1
0/3
0/4
0/1
Arboreal species
Ahaetulla ahaetulla
Ahaetulla caudolineata
Ahaetulla punctulata
Boiga dendrophila
Boiga irregulans
Chondropython viridis
Chrysopelea ornata
Dendrelaphis calligaster
Dendrelaphis punctulata
Dendrelaphis caudolineata
Dendrophis terrificus
Dryophis prasinus
Hoplocephalus stephensii
Ptyas korros
20
57
97.5
182
402
145
83.7
163
51
28
78.2
104
201
76
90.5
113
126
132
155
105
103
124
97
72.5
138
87.8
93
16
18
15
17
19
16
16
15
15
19
18
23
17
18
0
2
1
2
0
0.6
1
0
0/1
0/2
0/2
6/0
1/5
0/1
0/1
0/3
0/6
0/1
0/1
0/3
2/0
0/1
1
0.187
0.144
0.004
2
0.174
0.196
0.096
0.018
3
1
2
Viperids
Aghislrodon contortrix
Agkislrodon piscivorus
Bolhrops schlegeli
Cerastes sp.
Crolalus atrox
Crotalus cerastes
Crotalus mitchelh
Crotalus ruber
Crolalus viridis
*Lachesis muta
*Bothrops atrox
*Not included in Figure 1.
249
861
102
80.7
106
65
43.3
1,000
135
285
415
123
50
115
106
85.0
189
175
29
32
28
28
31
35
39
39
39
20
27
1
1
1
1
2
3/0
1/0
2/0
0/1
1/0
1/0
1/0
2/0
17/0
0/2
0/1
0.013
1
0.119
0.158
0.15
0.014
1
13