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RESEARCH ARTICLE
The king of snakes: performance and morphology of intraguild
predators (Lampropeltis) and their prey (Pantherophis)
David A. Penning
1,2,
*and Brad R. Moon
1
ABSTRACT
Across ecosystems and trophic levels, predators are usually larger
than their prey, and when trophic morphology converges, predators
typically avoid predation on intraguild competitors unless the prey is
notably smaller in size. However, a currently unexplained exception
occurs in kingsnakes in the genus Lampropeltis. Kingsnakes are able
to capture, constrict and consume other snakes that are not only larger
than themselves but that are also powerful constrictors (such as
ratsnakes in the genus Pantherophis). Their mechanisms of success
as intraguild predators on other constrictors remain unknown. To begin
addressing these mechanisms, we studied the scaling of muscle
cross-sectional area, pulling force and constriction pressure across
the ontogeny of six species of snakes (Lampropeltis californiae,
L. getula,L. holbrooki,Pantherophis alleghaniensis,P. guttatus and
P. obsoletus). Muscle cross-sectional area is an indicator of potential
force production, pulling force is an indicator of escape performance,
and constriction pressure is a measure of prey-handling performance.
Muscle cross-sectional area scaled similarly for all snakes, and there
was no significant difference in maximum pulling force among species.
However, kingsnakes exerted significantly higher pressures on their
prey than ratsnakes. The similar escape performance among species
indicates that kingsnakes win in predatory encounters because of their
superiorconstriction performance, not because ratsnakes have inferior
escape performance. The superior constriction performance by
kingsnakes results from their consistent and distinctive coil posture
and perhaps from additional aspects of muscle structure and function
that need to be tested in future research.
KEY WORDS: Constriction, Cross-sectional area, Force, Muscle,
Pressure, Scaling
INTRODUCTION
The structure and function of an organism relate in part to predatory
and anti-predator adaptations (Darwin, 1859; Wainwright, 1994).
Predators are generally larger than their prey (Arnold, 1993; Radloff
and Du Toit, 2004), and as prey increase in size relative to their
predators, they become less vulnerable to predation (Magalhães
et al., 2005). Furthermore, as trophic ranks (Holt et al., 1999)
converge between predators (i.e. intraguild competitors; Polis et al.,
1989), predators become less likely to attack prey greater than
25–50% of their own mass (Buskirk, 1999; Palomares and Caro,
1999; Wise, 2006). When the predator and prey are closely matched
in size and have similar feeding morphology, an attack can bring
such a high risk to the predator that it might be avoided entirely,
even if the benefits of successful predation would be high (Donadio
and Buskirk, 2006). However, some snakes consume intraguild prey
that are well matched in predatory abilities and in some cases are
even larger than themselves (Jackson et al., 2004).
Modifications of the feeding apparatus have allowed many snakes,
including ones that eat other snakes (ophiophagous), to incorporate
massive prey into their diets (Traill, 1895; Smith, 1910; Greene,
1997; Cundall and Greene, 2000; Jackson et al., 2004; Leong and
Shunari, 2010). Many ophiophagous snakes are venomous (Greene,
1997), effectively offsetting the risks associated with trophic
similarity between similarly sized combatants; often only a single
bite is needed to subdue prey. Non-venomous ophiophagous snakes
must use other prey-handling behaviors, such as constriction.
Kingsnakes (genus Lampropeltis Fitzinger 1843) are non-
venomous, constricting snakes that are well known for the ability to
consume other snakes (Ernst and Ernst, 2003), including ones that are
larger than themselves (Jackson et al., 2004). Surprisingly,
kingsnakes are able to capture, constrict and fully ingest other
snakes (such as ratsnakes in the genus Pantherophis Fitzinger 1843)
that seem well matched in predatory ability, in that they are effective
constrictors on some of the same kinds of rodents that kingsnakes eat.
Furthermore, the prey snake can be larger than the kingsnake (Ernst
and Ernst, 2003; Jackson et al., 2004). There is currently no known
mechanism that differentiates the abilities of these two constricting
snakes, yet kingsnakes always seem to subdue ratsnakes and ‘win’the
predatory encounter (Jackson et al., 2004). Here, we sought to
understand how this one-sided predation event is possible.
Morphology and physiology set the functional limitations on
predator–prey dynamics (Webb, 1986). Although both morphology
and physiology are important, behavior can determine the ways in
which morphological elements and physiological capacities are used
(Hertz et al., 1982). For snakes that use constriction behavior, predation
performance can be evaluated by measuring peak constriction pressure
(Moon, 2000; Moon and Mehta, 2007; Boback et al., 2015; Penning
et al., 2015; Penning and Dartez, 2016). Constriction pressure is a
biologically important measure of performance (Moon and Mehta,
2007) because it can determine the time needed to subdue the prey and
reduces the chances of prey escaping or causing injury to the snake.
Potential ways of escaping from a constriction coil include pulling out
of the coil, counter-constricting to make the aggressor release its coil,
and clawing or biting to gain release. Therefore, pulling force is a
potentially important measure of performance in snakes because it
indicates a snake’s ability to escape from the grip of a predator
(Lourdais et al., 2005). Geometric scaling offers testable apriori
expectations as to how force production scales with body size
(Pennycuick, 1992). Because muscle force is proportional to muscle
cross-sectional area (MacIntosh et al., 2006), we expect pulling force to
scale with snake body mass
0.66
.
Both predation (constriction pressure) and escape (pulling force)
performance are affected by the cross-sectional area (CSA) of
Received 2 August 2016; Accepted 7 January 2017
1
Department of Biology, University of Louisiana at Lafayette, Lafayette, LA 70504-
43602, USA.
2
Department of Biology and Environmental Health, Missouri Southern
State University, Joplin, MO 64801, USA.
*Author for correspondence (davidapenning@gmail.com)
D.A.P., 0000-0002-5368-9900
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© 2017. Published by The Company of Biologists Ltd
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Journal of Experimental Biology (2017) 220, 1154-1161 doi:10.1242/jeb.147082
Journal of Experimental Biology
muscle (Moon and Candy, 1997; Lourdais et al., 2005), and in
principle can use up to about half of a snake’s axial musculature
(e.g. all the muscles on the concave parts of a constriction coil or on
the concave parts of multiple axial bends used in pulling
movements). Larger snakes have more muscle CSA (Moon and
Mehta, 2007); therefore, changes in body size can be expected to
have significant effects on these measures of performance in snakes
(Moon and Mehta, 2007; Penning et al., 2015; Penning and Dartez,
2016). Although a priori expectations can be generated regarding
the scaling of muscle force (Pennycuick, 1992), constriction
pressure is much more variable (Moon and Mehta, 2007; Penning
et al., 2015; Penning and Dartez, 2016) and depends on the area of
contact and force exertion. It is not clear apriorihow the surface area
of contact should change with size during the dynamic interaction
between predator and prey (Penning et al., 2015). Given that the
relationship between constriction pressure and the surface area of
contact has not yet been quantified for snakes of any size, we do not
have enough information to generate testable hypotheses about the
predicted scaling of constriction pressure with body size. Although
constriction pressure and pulling force are distinct variables that are
typically related to different behaviors, theyare appropriate indicators
of predation and escape performance in snakes (Moon, 2000;
Lourdais et al., 2005; Moon and Mehta, 2007; Boback et al., 2015;
Penning et al., 2015; Penning and Dartez, 2016). Therefore, they can
be compared across species and sizes to understand the factors that
affect the outcome of this predator–prey interaction.
To understand how one constricting snake can capture, subdue
and consume another constricting snake with similar predatory and
defensive mechanisms, we quantified and compared muscle CSA,
and measures of predation performance and escape performance
across the ontogeny of two intraguild competitors, kingsnakes and
ratsnakes. We chose the study species based on previously
published work on intraguild predation in snake-eating snakes,
dietary records, and geographic distributions (Ernst and Ernst, 2003;
Jackson et al., 2004). We used three species of kingsnakes:
Lampropeltis californiae (Blainville 1835), Lampropeltis getula
(Linnaeus 1766) and Lampropeltis holbrooki (Stejneger 1903); and
three species of ratsnakes: Pantherophis alleghaniensis (Holbrook
1836), Pantherophis guttatus (Linnaeus 1766), and Pantherophis
obsoletus (Say 1823) (Pyron et al., 2013).
We address several questions about how form and function
change across ontogeny and differ between species (Lampropeltis
spp. and Pantherophis spp.). How does axial muscle CSA vary and
change with size in kingsnakes and ratsnakes? What constriction
pressures are exerted on prey and how do they change with size?
What pulling forces can these snakes produce during escape
attempts, and how do they change with size? We discuss several
possible mechanisms that can determine the winner of predatory
interactions between two constricting snakes.
MATERIALS AND METHODS
We chose our overall sample sizes based on available specimens and
previously published work for both morphological (Jayne and
Riley, 2007; Herrel et al., 2011) and performance investigations
(Moon and Mehta, 2007; Penning et al., 2015; Penning and Dartez,
2016). For each experiment below, we provide the sample size for
that specific experiment.
Morphology and scaling
We measured the morphology of 36 preserved snakes (4 L. holbrooki,
9L. getula,8P. guttatus and 15 P. obsoletus) from a teaching
collection (University of Louisiana at Lafayette) or the personal
collection of D.A.P. (20 females, 16 males). We lacked specimens for
measuring the morphology of L. californiae and P. alleghaniensis.
Weweighedeachsnakeandmeasureditssnout–vent length (SVL).
All specimens experienced similar fixation and preservation
durations. Although some tissue dehydration might have occurred,
the results would be consistent across all specimens (Herrel et al.,
2014). Because snakes are known to exhibit longitudinal variation in
external shape and in muscular anatomy (Nicodemo, 2012), we
quantified their muscle CSA along the body. Specifically, we cut each
specimen into sections at 20, 40, 60, 80 and 100% of its SVL (i.e.
down to the cloaca, based on our observationsthat the tail typically is
not involved in a constriction coil), photographed each cross-section,
and measured the anatomical CSA of major muscle groups (see
below). For small cross-sections, we used a Canon EOS Rebel
T5i digital camera attached to a Zeiss Stemi 2000-C stereoscopic
microscope, with the cross-sections immersed in 70% isopropyl
alcohol. For larger cross-sections, we used an Olympus Stylus Tough
TG-630 digital camera. Each photograph included a scale; we
confirmed that the images had square pixels, making a single scale
appropriate. We measured the muscle CSA of five epaxial muscles
(semispinalis–spinalis complex, multifidis, longissimus dorsi and
iliocostalis; Fig. 1) in each section of the body (following Jayne and
Riley, 2007; Herrel et al., 2011) using ImageJ software (NIH; https://
imagej.nih.gov/ij/) (following Herrel et al., 2011). We chose this
method of measuring muscle CSA to follow previous methods
(Lourdais et al., 2005; Jayne and Riley, 2007; Herrel et al., 2011) and
because a simple measure of external body width (a dimension of
length) would represent only half of the possible variation in muscle
cross-sectional area (length
2
); furthermore, previous work has shown
that although linear measuresare significantly related tomuscle cross-
sectional areas, they miss a considerable portion of the variation in
muscle cross-sectional area (Lourdais et al., 2005, found that R
2
=0.73
for this relationship).
Predation performance
All experimentation was approved by the University of Louisiana
at Lafayette’s Institutional Animal Care and Use Committee
(approval no. 2016-8717-006). We tested the constriction
performance of 182 snakes (21 L. californiae,12L. holbrooki,56
L. getula;21P. alleghaniensis,22P. guttatus and 50 P. obsoletus),
5 mm
Fig. 1. Anatomical cross-sections of kingsnakes and ratsnakes.
Photograph of anatomical cross-sections taken at 40% of snout–vent length for
a small kingsnake (left, Lampropeltis getula, 20.1 g) and ratsnake (right,
Pantherophis guttatus, 18.8 g). Major epaxial muscles are delineated with plain
gray (semispinalis–spinalis complex), plain white (multifidus), hatched white
(longissimus dorsi) and hatched gray (iliocostalis). Cross-sections of the liver
can be seen in the bottom right in both specimens, with the stomach to the left.
Photographs of 40% SVL were chosen based on image quality.
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RESEARCH ARTICLE Journal of Experimental Biology (2017) 220, 1154-1161 doi:10.1242/jeb.147082
Journal of Experimental Biology
encompassing 98 females and 84 males. Kingsnakes and ratsnakes
eat a variety of prey, but all frequently consume small mammals
(Ernst and Ernst, 2003). To compare constriction performance
between snakes, we fed all snakes pre-killed rodents (mass
ratio=15.2±0.6% snake mass, mean±s.e.m.) with an attached
pressure sensor. The prey sizes were within the normal range
reported in the literature from dietary records (Rodríguez-Robles,
2002) and previous work on constriction performance (Moon and
Mehta, 2007; Penning et al., 2015; Penning and Dartez, 2016).
Dead prey are commonly used to measure maximum constriction
pressures (Moon and Mehta, 2007; Penning et al., 2015; Penning
and Dartez, 2016), and manually simulating movements in dead
prey produces similar results to those from constriction of live prey
(Moon, 2000). We placed pressure sensors externally on the prey
and anchored them in place with wax-coated string; this placement
yielded similar sensitivities and outputs to internal placement of the
sensor (Penning and Dartez, 2016). For smaller snakes (<0.5 m), we
used a 0.5 ml water-filled latex balloon as the pressure sensor, and
for larger snakes we used a 2 ml water-filled rubber pipette bulb as
the pressure sensor. Both sensors are made of similarly compliant
materials that transmitted applied force to the transducer. In pilot
tests, both sensors produced accurate and repeatable results when
known forces were applied.
We connected the pressure sensor to a research-grade blood
pressure transducer (model 60-3002, Harvard Apparatus, Holliston,
MA, USA) and offered prey to each snake with long forceps. We
shook the prey to simulate movement and elicit a strong response
from each snake (following Moon and Mehta, 2007; Penning and
Dartez, 2016). Each snake participated in one to three constriction
trials and experienced simulated struggling for 5 min with limb and
body twitches approximately every 10 s. If we recorded multiple
constriction events from a single snake, we analysed the single
feeding event with the highest constriction pressure (Moon, 2000).
During the constriction event, we recorded peak constriction
pressure from the digital readout built into the transducer (which
had a refresh rate of 2 Hz) and the number of loops used in the
constriction coil. We report peak constriction pressure as the
response variable based on previously published methods (Moon
and Mehta, 2007; Penning et al., 2015; Penning and Dartez, 2016)
and our current experimental design. Constricting snakes are known
to respond to prey cues and will downregulate constriction
performance when prey movement ceases (Moon, 2000; Boback
et al., 2012). Because we offered pre-killed prey and controlled all
prey movements, we did not measure pressure exertion over time.
When we stopped simulating prey-struggling, all snakes responded
by reducing their constriction pressures. Once peak constriction
pressure began to decline, we removed the pressure sensor from the
prey and the snakes completed the feeding event. While snakes were
swallowing their prey, we measured their maximum diameters with
digital calipers (Series 500, Mitutoyo, Aurora, IL, USA).
Escape performance
We tested maximum pulling forces of 98 snakes (7 L. californiae,7
L. holbrooki,32L. getula;8P. alleghaniensis,6P. guttatus and 38
P. obsoletus) encompassing 53 females and 45 males. To measure
maximum pulling force, we anchored each snake to a large flat
surface using gaffer’s tape placed just behind the head. We attached
a Pesola scale (Rebmattli 19, CH-6340 Baar, Switzerland) to the
snake just anterior to the cloaca with gaffer’s tape. Pesola scales
showed no signs of drift when tested repeatedly over 5 min periods
with weights of approximately 50% of the total measurement
capacity of the scale. We chose the scale size for each snake based
on pilot data and with the capacity to measure twice the pulling-force
capacity of the snake (snake pulling force/scale force maximum=
51±3%). Further, Pesola scales provided similar and repeatable
results when calibrated against an isometric force transducer
(MLT500/A, AD Instruments, Colorado Springs, CO, USA).
Once the scale was attached, we manually straightened the snake
to its maximum length and anchored the spring scale with tape to the
flat surface. We then gently agitated the anchored snake to elicit a
pulling motion for 5 min (Lourdais et al., 2005, methodology
summarized in fig. 2). As the snake attempted to pull free from
linear subjugation, it pulled against the spring scale and displaced a
marker on the scale. We used a GoPro Hero 4 Black camera (GoPro,
Inc., San Mateo, CA, USA) to record spring scale displacements
during the pulling movements (720 pixel video at 60 frames s
–1
).
Using Tracker 4.87 software (Open Source Physics, http://www.
opensourcephysics.org/index.cfm), we advanced frame by frame
and recorded the maximum pulling force for each snake during its
5 min trial, and then converted the scale values from mass (g) to
pulling force (N).
Statistical analyses
We used log
10
-transformed data for all models. To quantify the
scaling of muscle CSA against body mass, we used reduced major
axis (RMA) regression (Smith, 2009). To test for differences in
slopes and elevations between kingsnakes and ratsnakes, we added
snake species as a categorical variable to the RMA regressions; this
is the RMA equivalent of ANCOVA (in the smatr 3 code package in
RStudio; Warton et al., 2012) and allows for comparisons between
slopes (factor A×factor B) and intercepts ( factor A+factor B) in
models with a categorical predictor. To evaluate constriction
performance, we used ordinary least-squares (OLS) multiple
regression with peak constriction pressure as the dependent
variable, and snake species, maximum body diameter and the
number of loops used in a coil as independent variables. To evaluate
pulling force, we used OLS multiple regression with pulling force as
the dependent variable, snake species as a categorical variable, and
snake body mass as the independent variable. Following previous
methods (Herrel et al., 2011; Penning, 2016) and the general
recommendations for regression analyses based on regression-line
symmetry (Smith, 2009), we used RMA regression for comparisons
between two morphological variables and OLS regression for
comparisons between one morphological and one performance
variable. We retained all data in all models because the results were
the same with all data retained and with outliers removed. All
statistical tests were considered significant when P<0.05. We
performed analyses in JMP Pro 11.0.0 (SAS Institute Inc., Cary,
NC, USA), RStudio (version 0.99.441; http://www.rstudio.com/),
and Past 3.08 (Hammer et al., 2001).
RESULTS
Morphological scaling
The five major epaxial muscles were easily delineated in most cross-
sections (Fig. 1). For 11 of the cross-sections, we had to confirm
muscle identities and boundaries with further probing and visual
inspection. Muscle cross-sectional areas varied at each position
along the body (Table 1). We did not have specimens available for
quantifying muscle CSA in L. californiae and P. alleghaniensis.
Muscle CSA increased with body mass in all cross-sections in all
species (Table 2); in most sections and species, CSA also scaled
with positive allometry (slope greater than 0.67). At each position
along the body, the slopes (mass×species interaction; Table 2)
and intercepts (mass+species) for muscle CSA did not differ
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RESEARCH ARTICLE Journal of Experimental Biology (2017) 220, 1154-1161 doi:10.1242/jeb.147082
Journal of Experimental Biology
significantly among species of Lampropeltis or Pantherophis (all
P>0.05; Table 2). Across ontogeny, muscle CSA at each location
increased similarly in all species (Table 2).
Predation performance
All snakes readily struck at and constricted rodent prey vigorously
using one to three loops of the body in a coil. Kingsnakes typically
constricted using a single posture (Fig. 2A), with multiple loops
forming a tight coil like that of a spring; 91% of the 89 kingsnakes
used such a coil. Peak constriction pressures were 5.3–41.6 kPa for
kingsnakes and 3.2–23.7 kPa for ratsnakes (Table 3). Ratsnake
constriction postures were much more variable than the typical
kingsnake posture, with loops placed at different positions and
angles on prey, loops that overlapped one another, and with the
ratsnake’s head inside or outside the coil (Fig. 2B). Of the 93
ratsnakes, only 5.4% used spring-like coils. Across all six species,
there was no significant difference between the number of loops
used in a coil (Kruskal–Wallis H=6.8, P>0.23; Table 3).
Starting with a full-factorial model ( pressure=diameter×number
of loops×species), we sequentially removed non-significant factors
to arrive at the final model ( pressure=diameter+number of loops+
species; F
7,174
=61.3, P<0.001, adjusted R
2
=0.70). Diameter
(F
1,174
=148.1, P<0.0001), number of loops (F
1,174
=9.88,
P<0.003) and species (F
5,174
=18.65, P<0.0001) were all
significant factors in the final model. Within each genus, there
were no significant pair-wise differences between covariate-
adjusted means for peak constriction pressure (Tukey’s HSD tests;
Fig. 3). However, kingsnakes constricted with higher pressures than
ratsnakes (Fig. 3).
To analyse the scaling of constriction performance across body
size the same way as in previous work (Moon and Mehta, 2007;
Penning et al., 2015; Penning and Dartez, 2016), we regressed
peak constriction pressure against snake diameter. Diameter
(F
1,175
=300.1, P<0.0001) and species (F
5,175
=18.4, P<0.0001)
were significant factors. The interaction (diameter×species) was not
significant (F
5,170
=0.38, P>0.8), resulting in a similar scaling
relationship between pressure and snake diameter for all six species
(overall β=0.88). As with the full model, there were no significant
differences between species in covariate-adjusted means within
each genus (Tukey’s HSD tests, all P>0.05). However, all
kingsnake means were significantly higher than all ratsnake
means (Tukey’s HSD tests, all P<0.05; Fig. 4).
Escape performance
In the tests of escape performance, snakes bent their bodies into
S-shaped curves and pulled against the Pesola scale inattemptsto free
themselves. Restrained snakes typically exerted their maximum
pulling forces <1.5 min into the 5 min trial. Maximum pulling forces
ranged from 0.9 to 24.5 N (Table 3). In a full model (pulling
force=mass×species), the interaction (F
5,86
=0.25, P>0.9) and species
factor (F
5,86
=2.1, P>0.068) were not significant. Removing the
interaction term did not result in a significant species effect,
producing a final model that included only pulling force and mass.
Larger snakes pulled with significantly higher forces than smaller
individuals, regardless of species (pulling force=0.69×mass–0.68;
F
1,96
=1967, R
2
=0.95, P<0.0001; Fig. 5). Maximum pulling force
scaled isometrically with body size (β=0.69; 95% CI=0.65–0.72).
DISCUSSION
Morphology and scaling
At every position sampled along the body, muscle CSA scaled
positively with body mass in both kingsnakes and ratsnakes, and
Table 1. Descriptive statistics of body mass and muscle cross-sectional area (CSA) in kingsnakes (Lampropeltis spp.) and ratsnakes (Pantherophis spp.)
Muscle CSA
Species NBody mass (g) 20% SVL 40% SVL 60% SVL 80% SVL 100% SVL
L. getula 4 32±13.8 (14–74) 0.07±0.04 (0.02–0.19) 0.065±0.02 (0.03–0.13) 0.06±0.02 (0.02–0.10) 0.04±0.008 (0.02–0.06) 0.02±0.005 (0.02–0.04)
L. holbrooki 9 272±91.8 (12–634) 0.37±0.11 (0.03–0.87) 0.39±0.12 (0.03–0.88) 0.36±0.12 (0.03–0.93) 0.32±0.10 (0.02–0.82) 0.15±0.05 (0.01–0.37)
P. guttatus 8 107±78.2 (9–652) 0.18±0.13 (0.036–1.05) 0.20±0.13 (0.04–1.12) 0.19±0.13 (0.04–1.05) 0.14±0.09 (0.03–0.77) 0.08±0.04 (0.015–0.37)
P. obsoletus 15 494±110 (14–1274) 0.55±0.11 (0.05–1.39) 0.66±0.13 (0.04–1.70) 0.72±0.15 (0.04–1.94) 0.69±0.16 (0.03–2.12) 0.36±0.08 (0.01–1.03)
Values are mean±s.e.m. with ranges in brackets.
Muscle CSA was measured in cm
2
at each position along the body (% of SVL).
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RESEARCH ARTICLE Journal of Experimental Biology (2017) 220, 1154-1161 doi:10.1242/jeb.147082
Journal of Experimental Biology
in most sections and species, muscle CSA scaled with positive
allometry (Table 2). The lack of significant differences between
species in muscle CSA and its scaling means that similarly sized
kingsnakes and ratsnakes have the same amount of muscle that can
be used in constriction or escape movements. However, there might
be differences in muscle physiological cross-sectional area (the area
of a muscle perpendicular to the muscle fibers), and hence
maximum force production, that we have not yet detected.
Predation and escape performance
In constriction, if we assume that the muscles on the concave side of
the coil contribute to force exertion, then up to half of the total
musculature can be used and contribute to the constriction pressure.
In a pulling-force test, if we assume that a snake bends into
sinusoidal curves and the musculature on the concave part of each
curve contributes to the pulling force, then up to half of the total
musculature can be used and contribute to the pulling force.
So although constriction pressure and pulling force are distinct
variables used in different behaviors, they are appropriate indicators
of predation and escape performance, and can be compared across
species and sizes to understand the factors that affect the outcome of
the predator–prey interaction that we studied.
Across ontogeny, all species increased constriction performance
in a similar manner (i.e. with similar slopes; Fig. 4). However, at
every body size, kingsnakes produced significantly higher
constriction pressures than identically sized ratsnakes. The similar
escape performance among species indicates that kingsnakes win
in predatory encounters because of their superior constriction
performance, not because ratsnakes have inferior escape
performance. What are some possible mechanisms of the superior
performance by kingsnakes?
With all snakes using a similar number of loops, the orientation of
loops in the coil might optimize muscle fiber orientations and force
transmission. Kingsnakes produced higher constriction pressures
for a given number of loops in a coil (Fig. 3), and had a more
uniform coil posture than ratsnakes (Fig. 2). It is possible that the
kingsnake coil posture might maximize the force applied (and
therefore pressure) to the prey by reducing the need for coil
adjustments and movements. Reducing the need for movements
might enable both isometric and tetanic contractions that maximize
force output, and could reduce periods of loosening that could allow
prey to struggle more or escape. It is also possible that kingsnake
Table 2. Species comparisons of the scaling relationships for muscle cross-sectional area (CSA) relative to body mass for kingsnake species
(Lampropeltis spp.) and ratsnake species (Pantherophis spp.)
Position (% of SVL) Species Slope Intercept R
2
Species×mass Species+mass
20 L. getula 1.25 (0.80, 1.94) –3.34 (–3.86, –2.22) 0.98 P>0.23 (4.3) P>0.53 (2.2)
L. holbrooki 0.80 (0.74, 0.86) –2.64 (–2.47, –2.21) 0.99 ––
P. guttatus 0.85 (0.69, 1.06) –2.76 (–2.76, –2.16) 0.95 ––
P. obsoletus 0.79 (0.73, 0.85) –2.64 (–2.49, –2.19) 0.98 ––
40 L. getula 0.95 (0.35, 2.53) –2.60 (–4.17, –1.02) 0.86 P>0.91 (0.52) P>0.63 (1.78)
L. holbrooki 0.79 (0.72, 0.85) –2.27 (–2.41, –2.13) 0.99 ––
P. guttatus 0.82 (0.64, 1.05) –2.32 (–2.67, –1.98) 0.94 ––
P. obsoletus 0.80 (0.73, 0.89) –2.31 (–2.51, –2.12) 0.97 ––
60 L. getula 0.83 (0.68, 0.98) –2.48 (–3.96, –1.00) 0.84 P>0.95 (0.31) P>0.18 (4.90)
L. holbrooki 0.87 (0.73, 1.03) –2.53 (–2.85, –2.20) 0.96 ––
P. guttatus 0.82 (0.68, 0.99) –2.35 (–2.60, –2.10) 0.97 ––
P. obsoletus 0.83 (0.76, 0.91) –2.36 (–2.54, –2.19) 0.98 ––
80 L. getula 0.63 (0.19, 2.07) –2.33 (–3.68, –0.97) 0.76 P>0.48 (2.47) P>0.39 (2.96)
L. holbrooki 0.88 (0.72, 1.09) –2.61 (–3.01, –2.22) 0.95 ––
P. guttatus 0.79 (0.62, 1.01) –2.41 (–2.72, –2.10) 0.94 ––
P. obsoletus 0.92 (0.86, 0.98) –2.63 (–2.77, –2.49) 0.99 ––
100 L. getula 0.55 (0.34, 0.88) –2.41 (–2.80, –2.02) 0.97 P>0.16 (5.12) P>0.39 (2.99)
L. holbrooki 0.85 (0.68, 1.07) –2.85 (–3.27, –2.43) 0.93 ––
P. guttatus 0.82 (0.68, 0.99) –2.76 (–3.01, –2.51) 0.97 ––
P. obsoletus 0.91 (0.85, 0.97) –2.88 (–3.28, –2.73) 0.99 ––
Values are based on reduced major axis regressions on log
10
data with snake species as a categorical variable (muscle CSA=species×mass). Slope and
intercept confidence limits (95%) are in parentheses. Comparisons between species for each section of the body are for differences between slopes
(species×mass) and elevations (species+mass), and are given by Pat each SVL site with test statistics in parentheses. Muscle CSA was measured in cm
2
and
mass in g.
A
B
Fig. 2. Constriction coil postures of kingsnakes and ratsnakes. Typical
constriction coil postures in a kingsnake, Lampropeltis getula (92 g; A), and
a ratsnake, Pantherophis guttatus (86 g; B). Both snakes were constricting
similarly sized mice, Mus musculus (12 g). The relative prey mass was 13% for
the kingsnake and 13.9% for the ratsnake.
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Journal of Experimental Biology
muscle might be able to exert higher forces than ratsnake muscle by
using different types of muscle contractions or by having different
muscle fiber angles and therefore higher physiological cross-
sectional areas. Furthermore, in seeking to escape, a ratsnake must
use shortening contractions, which exert lower forces than isometric
and tetanic contractions (MacIntosh et al., 2006). Additionally,
constriction bouts between kingsnakes and ratsnakes can last for
hours (Jackson et al., 2004), suggesting that muscle endurance
might be important. Measures of total pressure (the integral of
pressure versus time; Boback et al., 2015) delivered to both living
and dead prey could also reveal differences in whole-body
performance that have gone undetected here because we
artificially controlled prey movements. Further work is needed in
order to test these hypotheses. For example, experimental tests of
muscle contractile force and endurance would help identify
potential muscle-level differences between kingsnakes and
ratsnakes. Lastly, our measures of predation performance derive
from all snakes feeding on rodent prey. This was done because
ratsnakes are not known to commonly feed on other snakes.
Therefore, it is possible that other emergent factors might contribute
to the success of intraguild predation by kingsnakes that have gone
undetected in our comparisons of performance when all snakes were
fed rodent prey. There might be other ways in which ratsnakes are
poor competitors (or kingsnakes superior competitors) in this
ophiophagous context.
The effects of constriction pressure on prey animals
Constriction can disrupt breathing (McLees, 1928; Hardy, 1994)
and circulation (McLees, 1928; Hardy, 1994; Moon, 2000; Moon
and Mehta, 2007; Boback et al., 2015), cause structural damage to
the spine (Rivas, 2004; Moon and Mehta, 2007), cause internal
bleeding (Greene, 1983; Penning and Dartez, 2016), and potentially
disrupt brain function (Penning et al., 2015; Penning and Dartez,
2016). Although endotherms die quickly (within 10–78 s; McLees,
1928; Hardy, 1994) from constriction, ectothermic prey might be
only fatigued by constriction and swallowed alive (Hardy, 1994;
Boback et al., 2015). We have observed both escape by Anolis
lizards after extended constriction, and their death from constriction
in the same time taken to kill endothermic prey (∼1 min). Hence, the
effects of constriction on ectotherms are variable and potentially
complex; they might include harmful fluid movements, tissue
distortions or damage, and neurological disruptions (Greene, 1983;
Table 3. Descriptive statistics of body mass, diameter, SVL maximum pulling force, number of loops in a coil and peak constriction pressure in
kingsnakes (Lampropeltis spp.) and ratsnakes (Pantherophis spp.)
Species NMass (g) Diameter (cm) SVL (cm) Pulling force (N) Number of loops Constriction pressure (kPa)
Escape performance
L. californiae 7 258±88.0 (35–592) 2.1±0.33 (1.1–3.2) 72.3±10.9 (41–102) 9.2±2.7 (2.5–19.0) ––
L. getula 32 193±49.2 (17–1010) 1.8±0.14 (0.9–4.0) 61.5±4.4 (36–124) 6.3±1.1 (0.9–23.7) ––
L. holbrooki 7 159±41.4 (16–292) 1.75±0.18 (1.0–2.2) 67.0±9.6 (31–91) 7.4±1.8 (1.0–12.7) ––
P. alleghaniensis 8 77±43.9 (15–376) 1.4±0.23 (1.0–2.9) 49.1±7.7 (33–97) 3.9±1.6 (1.5–14.3) ––
P. guttatus 6 55±21.2 (19–125) 1.2±0.13 (0.9–1.8) 45.0±4.7 (34–61) 3.3±0.9 (1.8–6.6) ––
P. obsoletus 38 129±32.3 (10–778) 1.7±0.12 (0.8–3.6) 59.1±4.5 (30–136) 5.0±0.9 (0.8–24.5) ––
Constriction performance
L. californiae 21 189±30.1 (14–470) 1.8±0.14 (0.9–3.1) 73.1±5.9 (31–131) –2.1±0.2 (1–3) 22.5±1.9 (7.7–41.7)
L. getula 56 118±32.8 (11–1240) 1.4±0.09 (0.7–4.5) 50.8±3.5 (26–140) –2.0±0.1 (1–3) 17.1±1.1 (5.3–41.6)
L. holbrooki 12 168.3±33.1 (13–379) 1.8±0.19 (0.9–2.9) 72.7±7.3 (33–108) –2.3±0.2 (1–3) 20.8±1.7 (9.9–26.8)
P. alleghaniensis 21 37.2±17.3 (10–381) 1.1±0.09 (0.7–2.6) 40.5±3.5 (25–103) –1.8±0.1 (1–3) 8.9±0.6 (3.2–19.7)
P. guttatus 22 240.8±66.9 (6–980) 1.7±0.20 (0.8–3.5) 62.6±8.0 (22–114) –1.7±0.1 (1–3) 11.9±1.5 (3.2–23.7)
P. obsoletus 50 42.9±12.1 (7–562) 1.1±0.06 (0.7–2.9) 42.1±2.6 (23–112) –2.0±0.2 (1–3) 8.5±0.7 (3.2–17.3)
Values are mean±s.e.m. with data ranges in brackets. Number of loops was measured in decimal values of the number of complete loops (1/2 loop intervals).
0.85
0.95
1.05
1.15
1.25
L. californiae L. getula L. holbrooki P. alleghaniensis P. guttatus P. obsoletus
Species
a
b
1.30
log10 Peak constriction pressure (kPa)
1.20
1.10
1.00
0.90
Fig. 3. Peak constriction pressures of
kingsnakes and ratsnakes. Peak
constriction pressures (kPa) for six species
of snakes (kingsnakes, Lampropeltis spp.,
are black and ratsnakes, Pantherophis spp.,
are grey). Bars and lines indicate log-
transformed covariate-adjusted means±
s.e.m. for each species from a full model
(pressure=diameter+species+number of
loops). Significant differences (Tukey HSD,
all P<0.05) are denoted with different letters
(a,b). Sample sizes are as follows:
L. californiae N=21, L. getula N=56,
L. holbrooki N=12, P. alleghaniensis N=21,
P. guttatus N=22 and P. obsoletus N=50. The
total sample consists of 98 females and 84
males.
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Rivas, 2004; Moon, 2000; Moon and Mehta, 2007; Boback et al.,
2015; Penning et al., 2015; Penning and Dartez, 2016). This
variation and complexity indicate that we do not yet fully
understand the effects of constriction, particularly on ectothermic
prey. The constricting snakes probably also experience internal
pressures from the forces they exert on prey. However, blood
pressures rise only slightly during constriction in boas, and less than
during other behaviors such as hissing and swallowing (Wang et al.,
2001). Changes in a snake’s blood pressure during constriction are
not yet well known and might affect circulation to parts of their
musculature, but are clearly well tolerated by the constrictors. When
prey are constricted, they experience circumferential pressure that
could result in high internal pressures (Halperin et al., 1993; Boback
et al., 2015; Penning, 2016) that have different effects on internal
fluids than pressure applied at a specific point and that might be
different from what the constricting snake itself experiences.
When kingsnakes and their prey snakes are well matched in size,
our results show that the kingsnakes succeed in predation because
they have superior constriction performance. Our study also shows
that kingsnakes and their intraguild prey, ratsnakes, are comparable
in total muscular cross-sectional area and escape performance.
Although other aspects of the physiology of constriction still need to
be examined, we presume that superior constriction performance
results from their consistent and distinctive coil posture that we
have shown here. These constriction abilities allow kingsnakes
to succeed as intraguild predators on other snakes, including
constrictors larger than themselves.
Acknowledgements
We thank T. Lyon, M. Miles and L. Moberly for allowing access to their snakes, and
J. Albert, A. Herrel, P. Leberg and D. Povinelli for providing comments on earlier
drafts that helped improve the quality of the manuscript. D.A.P. thanks M. Fulbright,
L. Jones, I. Moberly, M. Perkins and B. Sawvel and for their helpful discussions, and
K. Smith and S. Fredericq for providing access to equipment and supplies. B.R.M.
thanks C. Gans, D. Hardy, N. Kley and S. Secor for valuable insights.
Competing interests
The authors declare no competing or financial interests.
Author contributions
D.A.P. collected and analysed all data, drafted the manuscript and provided funding.
B.R.M. helped design the project, edit the manuscript, provide several specimens
and provide funding. Both approved the final manuscript.
Funding
Partial funding was provided by the Louisiana Board of Regents ( grants RD-A-34
and ENH-TR-77 to B.R.M. and Doctoral Fellowship to D.A.P.), the National
Geographic Society (grant 7933-05 to B.R.M.), the National Science Foundation
(IOS-0817647 to B.R.M.), the Department of Biology and the Graduate Student
Organization at the University of Louisiana at Lafayette (to D.A.P.), the Louisiana
Department of Wildlife and Fisheries Rockefeller State Wildlife Scholarship (to
D.A.P.), the Kansas Herpetological Society (to D.A.P.), Miles of Exotics (to D.A.P.)
and BhB Reptiles (to D.A.P.).
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