Content uploaded by David Penning
Author content
All content in this area was uploaded by David Penning on Dec 11, 2017
Content may be subject to copyright.
SHORT COMMUNICATION
The big squeeze: scaling of constriction pressure in two of the
world’s largest snakes, Python reticulatus and Python molurus
bivittatus
David A. Penning
‡
, Schuyler F. Dartez* and Brad R. Moon
ABSTRACT
Snakes are important predators that have radiated throughout many
ecosystems, and constriction was important in their radiation.
Constrictors immobilize and kill prey by using body loops to exert
pressure on their prey. Despite its importance, little is known about
constriction performance or its full effects on prey. We studied the
scaling of constriction performance in two species of giant pythons
(Python reticulatus and Python molurus bivittatus) and propose a
new mechanism of prey death by constriction. In both species, peak
constriction pressure increased significantly with snake diameter.
These and other constrictors can exert pressures dramatically higher
than their prey’s blood pressure, suggesting that constriction can stop
circulatory function and perhaps kill prey rapidly by over-pressurizing
the brain and disrupting neural function. We propose the latter ‘red-
out effect’as another possible mechanism of prey death from
constriction. These effects may be important to recognize and treat
properly in rare cases when constrictors injure humans.
KEY WORDS: Burmese python, Feeding, Predator–prey, Predation,
Red-out effect, Reticulated python
INTRODUCTION
Constriction behaviour was probably very important in the
evolution and radiation of snakes, allowing for the subjugation of
otherwise unobtainable prey, including large and potentially
dangerous ones such as alligators, deer and, rarely, humans
(Greene and Burghardt, 1978; Murphy and Henderson, 1997).
Constricting snakes exert pressure by coiling around and squeezing
their prey, typically killing it before swallowing (Moon and
Mehta, 2007). Constriction takes energy and time, and risks
injury to the snake (Murphy and Henderson, 1997; Moon and
Mehta, 2007). Constriction performance is important because it can
affect feeding success, and hence growth and fitness (Moon and
Mehta, 2007).
Constriction pressures are generated by forces from the snake’s
axial musculature applied to the prey. These forces are proportional
to the cross-sectional area of active muscle, and therefore to snake
diameter (Moon and Mehta, 2007). Force production during
constriction may also be increased by using more of the body
because the segmental axial muscles act mainly in parallel (Moon
and Mehta, 2007). As snakes increase in size, so should their peak
constriction pressures. However, constriction involves a dynamic
interaction between predator and prey, and can have highly variable
outcomes. Despite the widespread use of constriction, the cause of
death during constriction has been uncertain; it may involve several
non-exclusive mechanisms including suffocation, circulatory arrest
or spinal injury (reviewed by Moon and Mehta, 2007). Moon (2000)
first tested the possibility that constriction causes circulatory arrest
and demonstrated that constriction pressure can be substantially
higher than the systolic blood pressure of mice that are eaten by
constrictors. Later, Moon and Mehta (2007) tested snakes of
different species and sizes, and inferred that low pressures may
cause suffocation, moderate pressures may cause circulatory arrest,
and extremely high pressures may cause spinal injury. Boback et al.
(2015) nicely extended this earlier work by directly measuring
circulatory function in rats during constriction; they showed that a
constriction pressure of 20 kPa can severely impede cardiac and
circulatory function in rats. In the prey, heart rate decreased, cardiac
electrical activity became abnormal, and blood pressure increased
ca. sixfold in the vena cava near the heart and decreased by half
peripherally in the femoral artery, all indicating that constriction can
induce circulatory arrest (Boback et al., 2015). However, to our
knowledge, no previous work has tested the effects of constriction
pressure on neural tissue, one of the most immediately important
tissue systems in the prey.
Giant snakes have fascinated humans for centuries (Murphy and
Henderson, 1997). Despite such intense curiosity and ongoing
study, we have yet to fully understand how these animals work,
especially as predators. Snakes in the genus Python are typically
highly stereotyped constrictors (Greene and Burghardt, 1978) and
vary dramatically in body size. For example, both reticulated
pythons (Python reticulatus) and Burmese pythons (Python
molurus bivittatus) are born ca. 100–200 g in mass and 45 cm in
length, and can reach maximum lengths of 8–10 m (Murphy and
Henderson, 1997) and exceed 60 kg (this study). Accompanying
this dramatic growth are shifts in reproductive output, energy stores,
prey base, habitat use and other variables (Shine et al., 1998).
However, to our knowledge, no data are available on predatory
performance in either of these giant snakes, and no study has
evaluated intraspecific scaling of constriction performance for any
snake species. Here, we describe the ontogeny of constriction
performance in reticulated and Burmese pythons and discuss how it
relates to interspecific data from the literature. Lastly, we discuss the
implications of our findings for the cause of prey death during
constriction.
MATERIALS AND METHODS
This research was approved by the University of Louisiana at Lafayette’s
Institutional Animal Care and Use Committee. We tested 65 snakes in the
collections of private breeders. Python reticulatus Schneider 1801 (N=48)
Received 26 June 2015; Accepted 26 August 2015
Department of Biology, University of Louisiana at Lafayette, Lafayette, LA 70504-
43602, USA.
*Present address: Louisiana Department of Wildlife and Fisheries, White Lake
Wetlands Conservation Area, Gueydan, LA 70542, USA.
‡
Author for correspondence (davidapenning@gmail.com)
3364
© 2015. Published by The Company of Biologists Ltd
|
Journal of Experimental Biology (2015) 218, 3364-3367 doi:10.1242/jeb.127449
Journal of Experimental Biology
were 0.84–5.5 m long (snout–vent length, SVL) and 1.2–18.0 cm maximum
diameter. Python molurus bivittatus Kuhl 1820 (N=17) were 0.83–3.7 m in
SVL and 3.6–15.5 cm diameter. All snakes were fed live or recently killed
prey (Rattus norvegicus and Oryctolagus cuniculus) with an attached
pressure sensor. Prey type and size depended upon the owner’s feeding
regimen. Whenever we fed snakes pre-killed prey, we shook the prey with
forceps or tongs to simulate activity and elicit maximal constriction
performance (following Moon and Mehta, 2007).
For smaller snakes, we used a 2 ml water-filled rubber pipette bulb
attached to the prey as a pressure sensor, connected to a Research Grade
Blood Pressure Transducer (Model 60-3002, Harvard Apparatus, Holliston,
MA, USA). For larger snakes, we used either a Pressure Manometer (Model
SYS-PM100R, World Precision Instruments, Sarasota, FL, USA) with a
water-filled 100 ml rubber pipette bulb as the sensor, or an Omega
Instrument Remote Sensor attached to a DPI 705 Digital Pressure Indicator
(Omega Engineering, Inc., Stamford, CT, USA) with an air-filled Inflatable
Dent Remover Pad (Model LT-800, 20.32×20.32 cm, Lock Technology,
Inc., Naperville, IL, USA) as the sensor. We loosely attached sensors to the
prey’s thoracic region with string, hook-and-loop straps, or tape. Once we
instrumented the prey, we placed it in proximity to the snake. Snakes readily
struck at, constricted and consumed their prey. We recorded peak
constriction pressure (kPa), the number of loops used during constriction,
and maximum snake diameter. We removed the pressure sensor when the
snake began to swallow.
To assess constriction performance, we analysed the scaling of peak
constriction pressure using least-squares multiple linear regression with
peak pressure as the dependent variable and snake diameter and number
of loops in a coil as independent variables (all non-transformed data).
We also log-transformed our data and used t-tests to compare our
regression coefficients to interspecific values from Moon and Mehta
(2007). We performed analyses in R Studio and Past 3, and removed
non-significant factors to arrive at the final models (considered
significant at P<0.05).
RESULTS AND DISCUSSION
Reticulated and Burmese pythons both constricted the prey
vigorously using coils of 1–4 loops (Fig. 1). Reticulated pythons
exerted maximum pressures of 8.27–53.77 kPa, with larger
individuals exerting significantly higher peak pressures than
smaller individuals (constriction pressure=15.17+diameter×1.39;
R
2
=0.29, F
1,46
=19.06, P<0.0001; Fig. 1). Burmese pythons
constricted with maximum pressures of 18.0–42.93 kPa, with
larger individuals exerting significantly higher peak pressures than
smaller individuals (constriction pressure=17.7+diameter×1.42;
R
2
=0.61, F
1,15
=26.56, P<0.0002; Fig. 1). In a multiple linear
regression with a species×diameter interaction (overall F
3,61
=9.325,
P<0.0001), the slopes (interaction t=0.04, P>0.96) and intercepts
(t=0.43, P>0.66) did not differ significantly between these species.
The number of loops in a coil did not significantly affect peak
pressure in either species (reticulated t=0.42, P>0.6; Burmese
t=0.32, P>0.7), in contrast to the results of Moon and Mehta (2007).
Reticulated and Burmese pythons used a broader range of loops than
other species (1–2 loops were reported by Moon and Mehta, 2007),
and it seems likely that the pattern observed across multiple species
is not a reliable predictor of behaviour within any one of the species.
It is also possible that different loops within a coil exert different
forces, and hence contribute differently to the overall pressure
experienced by the prey. For example, one loop may exert maximum
force while others hold the prey in place, preventing escape but not
exerting maximum force.
Log-transformed constriction pressure in both species scaled
with significantly lower slopes (β
reticulated
=0.25, β
Burmese
=0.33)
than the interspecific data reported by Moon and Mehta (2007;
β=1.39; t
46
=13.21, P<0.0001 and t
15
=11.24, P<0.0001,
respectively; Fig. 2). The lower slopes within species than
between species could result from several factors. Constriction
requires muscle exertion, and therefore energy; so snakes may
modulate their effort and use submaximal but fully sufficient
performance, conserving energy in the process. For example, one
of our smallest snakes was capable of generating pressures
comparable to those of some of the largest pythons tested
(Fig. 1), suggesting that the larger pythons were not using their
maximum capacities to subdue prey. However, a large snake has
a large diameter, and therefore a larger surface area over which it
exerts force, although the relationships among force, surface area
and pressure are not yet well quantified in snakes. It is possible
that larger snakes exert maximum force during constriction, but
the area over which it is exerted on the prey results in lower
overall pressure. Reticulated and Burmese pythons were not
available for the interspecific study by Moon and Mehta (2007),
and the species they used were not available in sufficient
numbers for this study. When comparing individual
performance, the pressures generated by small reticulated and
Burmese pythons (<6 cm in diameter) are similar to those of
small pythons reported by Moon and Mehta (2007). Moon and
Mehta (2007) reported constriction pressures of four snakes with
diameters >7 cm; we recorded pressures from 34 snakes with
diameter >7 cm. The incorporation of more large snakes from
additional species would result in a different interspecific scaling
A
4 cm
0
50
100
150
200
250
300
350
400
450
0
10
20
30
40
50
60
0 5 10 15 20
Peak constriction pressure (mmHg)
Peak constriction pressure (kPa)
Snake diameter (cm)
Loops
1
2
3
4
Reticulated python
Burmese python
B
Fig. 1. Constricting pythons coil around and squeeze prey animals, which
exerts pressure on the prey that scales positively with snake diameter.
(A) A 1081 g juvenile Burmese python (Python molurus bivittatus) constricting
alabrat(Rattus norvegicus) weighing 99 g. (B) The scaling relationship
between peak constriction pressure and snake diameter. See Results and
Discussion for description of the regression model.
3365
SHORT COMMUNICATION Journal of Experimental Biology (2015) 218, 3364-3367 doi:10.1242/jeb.127449
Journal of Experimental Biology
exponent. Furthermore, relative meal size decreased in larger
snakes because larger prey were not available, although previous
work had the same limitation. Lastly, these differences may arise
from as yet unidentified factors. Despite the different scaling
results between studies, the constriction pressures generated by
all snakes were effective in killing their prey quite rapidly.
Although the constriction pressures exerted by reticulated and
Burmese pythons scale differently from those of other snakes,
many of the highest pressures (ca. 52 of the 65 data points) were
probably high enough to force blood into the brain at high
pressure in mammalian prey (Fig. 2).
In addition to suffocation, circulatory arrest and spinal
dislocation, we propose the ‘red-out effect’(Balldin, 2002) as a
fourth possible mechanism of prey death by constriction. The red-
out effect describes the effect of negative gravity on jet pilots during
extreme flight manoeuvres, in which vision becomes reddened by
uncontrollable blood flow to the brain and eyes (Balldin, 2002).
When fighter pilots experience negative gravitational accelerations
(G-forces), they incur a rush of blood to the brain that causes rapid
loss of consciousness (Balldin, 2002). Constriction pressures above
the venous blood pressure of the prey will impede blood flow and
oxygen delivery to tissues (reviewed by Moon and Mehta, 2007;
Boback et al., 2015). Constriction pressures dramatically higher
than the prey’s blood pressure could force blood away from the site
of constriction and into the extremities, including the head and
brain. We recorded maximum pressures of ca. 55 kPa from
reticulated and Burmese pythons, and previous work has recorded
pressures as high as 175 kPa (Moon and Mehta, 2007). Both of
these values are well above the normal blood pressures of mammals
(Flindt, 2003). Blood being pushed into the brain during peak
constriction exertion could cause the same red-out effect described
above for pilots, and could cause extensive ruptures in cranial blood
vessels.
Accompanying forced haemorrhaging caused by high
constriction pressures is the potential for immediate neural
disruption and damage. Interfering with the nervous system of
prey hinders their defensive capabilities, further reducing the
risk of injury to the snake. Neural tissue is sensitive to pressure
and can deform, tear and cease function entirely (Toth et al.,
1997; Courtney and Courtney, 2009). Shockwave and
concussive-impact pressure effects on the brain cause neural
damage and failure when in the range of 55–300 kPa during
transient exposures (Courtney and Courtney, 2009). Directed
pressures of ca. 140 kPa for only 20 ms on the dura of rats
causes immediate incapacitation for 120–200 s (Toth et al.,
1997), although lower pressures comparable to those we
recorded during constriction were not tested. Pressure is
probably not a localized phenomenon that dissipates near
impact sites, but can travel through tissues and structures from
the site of impact (e.g. constriction coil) to the neural tissue,
damaging it and perhaps immediately stopping function
(Courtney and Courtney, 2009).
Most pythons in this study exerted lower pressures than those
reported in the literature on brain impacts, although several
reached the lower range of damagingly high pressures, and other
snakes can exert pressures up to ca. 175 kPa (Moon and Mehta,
2007). Pressure-wave impacts occur over milliseconds, whereas
snakes constrict for orders of magnitude longer. Based on our
current knowledge of how pressure affects tissues, it is likely that
high constriction pressures are capable of interfering with, or
completely disabling, both circulatory and neural function (Toth
et al., 1997; Moon, 2000; Moon and Mehta, 2007; Courtney and
Courtney, 2009; Boback et al., 2015). The world’s largest snakes
are capable of quickly incapacitating large and potentially
dangerous prey by causing multiple kinds of injuries. The
dynamic interactions, movements and resulting postures that
occur during predation probably determine which kinds of injury
occur, are most severe, and subdue the prey most rapidly.
Furthermore, these diverse effects may be important to recognize
and treat properly in those rare cases when large constrictors
injure humans.
Acknowledgements
We thank B. Clark, M. Miles and N. McCorkendale for allowing access to their
snakes, and P. Leberg for help with experimental and analytical design. D.A.P.
thanks B. Sawvel and M. Perkins for helpful discussions. S.F.D. thanks L. Dartez,
C. Denesha, A. Rabatsky and P. Hampton for support and guidance. B.R.M. thanks
C. Gans, D. Hardy and N. Kley for valuable insights, and W.Boggs and D. Hamlin for
critical help with equipment.
Competing interests
The authors declare no competing or financial interests.
Author contributions
All three authors helped design the project, collect and analyse data, write the
manuscript, and provide funding. For data collection, D.A.P. tested P. m. bivittatus,
and S.F.D. and B.R.M. tested P. reticulatus. All authors approved the final
manuscript.
Funding
Funding was provided by the Louisiana Board of Regents Graduate Fellowship to
D.A.P., Graduate Student Organization at the University of Louisiana at Lafayette
to D.A.P., the Kansas Herpetological Society to D.A.P., University of Louisiana at
Lafayette Master’s Fellowship to S.F.D., personal funds by S.F.D., and the National
Geographic Society (grant number 7933-05 to B.R.M.).
References
Balldin, U. (2002). Acceleration effects on fighter pilots. In Medical Aspects of Harsh
Environments, Vol. 2 (ed. K. Pandoff and R. Burr), pp. 1014-1027. Virginia:
Department of the Army.
Boback, S. M., McCann, K. J., Wood, K. A., McNeal, P. M., Blankenship, E. L.
and Zwemer, C. F. (2015). Snake constriction rapidly induces circulatory arrest in
rats. J. Exp. Biol. 218, 2279-2288.
Courtney, A. C. and Courtney, M. W. (2009). A thoracic mechanism of mild
traumatic brain inju ry due to blast pressure waves. Med. Hypotheses 72,
76-83.
Flindt, R. (2003). Amazing Numbers in Biology. Berlin: Springer-Verlag.
Greene, H. W. and Burghardt, G. M. (1978). Behavior and phylogeny: constriction
in ancient and modern snakes. Science 200, 74-77.
Moon, B. R. (2000). The mechanics and muscular control of constriction in gopher
snakes (Pituophis melanoleucus) and a king snake (Lampropeltis getula). J. Zool.
Lond. 252, 83-98.
1.35
1.85
2.35
2.85
3.35
3.85
0.5
1
1.5
2
2.5
3
0 0.2 0.4 0.6 0.8 1 1.2
log pressure (mmHg)
log pressure (kPa)
log diameter (cm)
Reticulated python (N=48)
Burmese python (N=17)
Fig. 2. Constriction pressure scales differently in Python reticulatus and
P. molurus bivittatus than in other species. The interspecific slope (dashed
line) from Moon and Mehta (2007) represents 30 snakes from 12 species,
ranging in size from 0.85 to 12.5 cm in diameter. Blood pressure values (top
green bar, systolic; bottom blue bar, diastolic) are from mice, rats, rabbits,
sheep and humans (Flindt, 2003).
3366
SHORT COMMUNICATION Journal of Experimental Biology (2015) 218, 3364-3367 doi:10.1242/jeb.127449
Journal of Experimental Biology
Moon, B. R. and Mehta, R. S. (2007). Constriction strength in snakes. In Biology of
the Boas and Pythons (ed. R. W. Henderson and R. Powell), pp. 206-212. Utah:
Eagle Mountain Publishing.
Murphy, J. C. and Henderson, R. W. (1997). Tales of Giant Snakes: A Historical
Natural History of Anacondas and Pytho ns. Florida: Krieger Publishing
Company.
Shine, R., Harlow, P. S., Keogh, J. S. and Boeadi, (1998). The allometry of life-
history traits: insights from a study of giant snakes (Python reticulatus). J. Zool.
Lond. 244, 405-414.
Toth, Z., Hollrigel, G. S., Gorcs, T. and Soltesz, I. (1997). Instantaneous
perturbation of dentate interneuronal networks by a pressure wave-transient
delivered to the neocortex. J. Neurosci. 17, 8106-8117.
3367
SHORT COMMUNICATION Journal of Experimental Biology (2015) 218, 3364-3367 doi:10.1242/jeb.127449
Journal of Experimental Biology
