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Size, but not experience, affects the ontogeny of constriction performance in ball pythons (Python regius)

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Constriction is a prey-immobilization technique used by many snakes and is hypothesized to have been important to the evolution and diversification of snakes. However, very few studies have examined the factors that affect constriction performance. We investigated constriction performance in ball pythons (Python regius) by evaluating how peak constriction pressure is affected by snake size, sex, and experience. In one experiment, we tested the ontogenetic scaling of constriction performance and found that snake diameter was the only significant factor determining peak constriction pressure. The number of loops applied in a coil and its interaction with snake diameter did not significantly affect constriction performance. Constriction performance in ball pythons scaled differently than in other snakes that have been studied, and medium to large ball pythons are capable of exerting significantly higher pressures than those shown to cause circulatory arrest in prey. In a second experiment, we tested the effects of experience on constriction performance in hatchling ball pythons over 10 feeding events. By allowing snakes in one test group to gain constriction experience, and manually feeding snakes under sedation in another test group, we showed that experience did not affect constriction performance. During their final (10th) feedings, all pythons constricted similarly and with sufficiently high pressures to kill prey rapidly. At the end of the 10 feeding trials, snakes that were allowed to constrict were significantly smaller than their non-constricting counterparts. J. Exp. Zool. 9999A:XX-XX, 2016. © 2016 Wiley Periodicals, Inc.
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Size, But Not Experience, Affects
the Ontogeny of Constriction
Performance in Ball Pythons
(
Python regius
)
DAVID A. PENNING*
AND SCHUYLER F. DARTEZ
Department of Biology, University of Louisiana at Lafayette, Lafayette, Louisiana
Smaller organisms typically face greater competitive and
predation pressures than their larger counterparts (Carrier,
'96). This differential selective pressure can lead to juvenile
organisms being capable of high levels of performance to offset
their size disadvantage (Herrel and Gibb, 2006). If juveniles are
unable to achieve high levels of performance, some will use
different behaviors than adults in order to accomplish similar
goals. For example, juveniles may use different modes of
locomotion or habitats (Irschick et al., 2000), perform closer to
their maximum capacity (Irschick, 2000), or feed on different
prey (Herrel and Gibb, 2006). This behavioral exibility can be
an important component of the organism's phenotype (Mehta
and Burghardt, 2008). However, some organisms lack the
behavioral plasticity to employ different behaviors (Greene and
ABSTRACT Constriction is a prey-immobilization technique used by many snakes and is hypothesized to have
been important to the evolution and diversication of snakes. However, very few studies have
examined the factors that affect constriction performance. We investigated constriction
performance in ball pythons (Python regius) by evaluating how peak constriction pressure is
affected by snake size, sex, and experience. In one experiment, we tested the ontogenetic scaling of
constriction performance and found that snake diameter was the only signicant factor
determining peak constriction pressure. The number of loops applied in a coil and its interaction
with snake diameter did not signicantly affect constriction performance. Constriction
performance in ball pythons scaled differently than in other snakes that have been studied,
and medium to large ball pythons are capable of exerting signicantly higher pressures than those
shown to cause circulatory arrest in prey. In a second experiment, we tested the effects of
experience on constriction performance in hatchling ball pythons over 10 feeding events. By
allowing snakes in one test group to gain constriction experience, and manually feeding snakes
under sedation in another test group, we showed that experience did not affect constriction
performance. During their nal (10th) feedings, all pythons constricted similarly and with
sufciently high pressures to kill prey rapidly. At the end of the 10 feeding trials, snakes that were
allowed to constrict were signicantly smaller than their non-constricting counterparts. J. Exp.
Zool. 9999A:XXXX, 2016. ©2016 Wiley Periodicals, Inc.
How to cite this article: Penning DA, Dartez SF. 2016. Size, but not experience, affects the
ontogeny of constriction performance in ball pythons (Python regius). J. Exp. Zool. 9999A:XX
XX.
J. Exp. Zool.
9999A:XXXX,
2016
Conflicts of interest: The authors declare no conflicts of interest.
Current address: Schuyler F. Dartez's current address is Louisiana,
Department of Wildlife and Fisheries, White Lake Wetlands Conservation
Area, Gueydan, LA 70542.
Correspondence to: David A. Penning, Department of Biology,
University of Louisiana at Lafayette, Lafayette, LA 70504-43602.
E-mail: davidapenning@gmail.com
Received 8 December 2015; Revised 23 January 2016; Accepted 25
January 2016
DOI: 10.1002/jez.2007
Published online XX Month Year in Wiley Online Library
(wileyonlinelibrary.com).
RESEARCH ARTICLE
©2016 WILEY PERIODICALS, INC.
Burghardt, '78), relegating all individuals, regardless of their
size, to the same behavior. For these stereotyped behaviors,
body size likely has a strong inuence on performance
throughout ontogeny.
Constriction likely played a key role in the evolution and
radiation of snakes (Greene and Burghardt, '78), making it an
evolutionarily and functionally important mechanism of prey
handling. Constriction movements vary among snakes, and in
general are produced by a highly complex muscletendon system
(Mosauer, '35; Moon, 2000; Moon and Mehta, 2007) and involve
muscle contractions that exert pressure on the prey (Greene and
Burghardt, '78; Greene, '97). Constriction pressures have been
hypothesized to prevent breathing (McLees, '28), cause circulatory
arrest (Hardy, '94; Moon, 2000; Moon and Mehta, 2007; Boback
et al., 2015), and spinal damage (Rivas, 2004). High constriction
pressures have also been hypothesized to force blood towards the
brain and disrupt its function(Penning et al., 2015), a phenomenon
known to occur when pilots experience brief blood pooling in the
head (i.e. the red-out effect; Balldin, 2002; Williams et al., 2008).
Constriction postures vary among snake lineages (Greene and
Burghardt, '78) and ontogenetically within some lineages (Mori
'94; Mehta 2003, 2009). Mori ('94) and Mehta (2003) showed that
hatchling colubrid snakes are less effective than adults at forming
constriction coils, and argued that experience may be necessary
for procient coiling and rapid subjugation of prey. However, this
may not be the case in booid snakes, because they are typically
more stereotyped in their constriction behaviors than colubrid
snakes (Greene and Burghardt, '78), although some booid snakes
may exhibit more plasticity than previously thought (Mehta and
Burghardt, 2008).
The abilities of young snakes to improve their constriction
performance rapidly may have consequences for growth because
constriction requires energy, time, and risks of injury (Cruz-Neto
et al., 2001; Canjani et al., 2003; Moon and Mehta, 2007).
However, for snakes that display little behavioral variation,
constriction performance may be more dependent upon their size
than on past experience with prey. To our knowledge, only one
study has evaluated intraspecic scaling of constriction pressures
in snakes (Penning et al., 2015), and the results differed
signicantly from those on interspecic scaling (Moon and
Mehta, 2007). The scaling exponent for constriction performance
in two species of large pythons (Python molurus bivittatus and
Python reticulatus) was lower than in previous interspecic
comparisons (Moon and Mehta, 2007; Penning et al. 2015). Here,
we evaluate the effects of size, sex, and prior experience on
constriction performance in ball pythons (Python regius), and
compare our results to previous work. In the rst experiment, we
used a large sample size to test the ontogenetic scaling of
constriction performance in ball pythons. In a second experi-
ment, we used multiple clutches of snakes to test the effects of
experience on constriction performance in hatchling ball pythons
over 10 feeding events.
MATERIALS AND METHODS
This research was approved by the University of Louisiana at
Lafayette's Institutional Animal Care and Use Committee. For the
scaling experiment, we used ball pythons (Python regius;N¼40)
ranging from 0.062 kg to 2.8 kg in mass, 42.3cm to 153.6 cm in
snoutvent length (SVL), and 2.0 cm to 8.2 cm in maximum
diameter. Our sample size was determined by the number of
animals available to us in ve private collections. We fed snakes
live and pre-killed rodents (Mus musculus and Rattus norvegicus)
ranging from 2% to 13% of the snake's mass (7.5 0.63%,
mean s.e.m.) based on the owner's feeding regimen. Using
masking tape and duct tape, we attached to each rodent a water-
lled 2 mL rubber pipette bulb that was connected via exible
tubing to a Harvard Apparatus Research Grade Blood Pressure
Transducer (Model 60-3002, Harvard Apparatus, Holliston, MA,
USA). In a pilot study, internal and external sensors produced
similar results, and both internal (Moon, 2000; Boback et al.,
2012, 2015) and external (Mehta, 2005; Moon and Mehta, 2007;
Penning et al., 2015) sensors have been used to measure
constriction performance. For pre-killed prey, we systematically
shook the prey using long forceps in order to elicit maximal
constriction effort. Both live and dead prey can elicit powerful
constriction, particularly if dead prey are manually moved to
simulate a struggling response (Moon, 2000; Boback et al., 2012).
During constriction, we counted the number of loops in the coil,
and after the snake released the coil, but before it swallowed the
prey, we measured maximum snake diameter. We removed the
tape and bulb as soon as a coil was released, and all snakes
completed the feeding event.
We used multiple ordinary least-squares (OLS) regression to
analyze the scaling of constriction performance (Smith, 2009).
Peak constriction pressure was the dependent variable, and
snake size (diameter) and the number of loops in the
constriction coil were independent variables. We removed
non-signicant factors (number of loops used in a coil) from
the analyses and arrived at the nal model that included only
peak pressure and snake diameter. To evaluate potential
differences between sexes while controlling for the effect of
size, we added sex as a categorical variable to the regression
and tested for differences in the slopes and intercepts between
males and females. To compare our scaling results to previously
published results, we used t-tests on OLS regression slopes from
log-transformed data (Zar, '84).
For the experiment on experience and growth, we used
hatchling ball pythons (N¼22) from eight separate clutches. At
the onset of trials, snakes ranged in mass from 45.5 g to 72.6 g and
in SVL from 41.4 cm to 48.3 cm. All of the snakes were na
ıve to
prey and had no constriction experience prior to the trials. Snakes
were randomly assigned to one of two feeding categories: snakes
that would gain experience with prey-handling through time
(constricting group) and a control group that would not use
prey-handling behaviors (non-constricting group). Snakes in
2PENNING AND DARTEZ
J. Exp. Zool.
the two groups were not signicantly different in mass at the
beginning of trials (non-constricting group ¼59.4 2.2 g; con-
stricting group ¼55.1 1.8 g; t
20
¼1.1, P>0.14). We fed all
snakes pre-killed mice for the duration of the experiment, and
controlled relative prey mass (the ratio of prey mass to snake
mass) at ca. 10% (non-constricting group ¼9.1 0.31%; con-
stricting group ¼10.8 0.51%). For the constricting group, we
used the methods described above for the scaling experiment. We
fed each snake one meal per week for 10 weeks, allowing them to
gain both constriction experience and mass under natural
conditions. In rare cases in which the snakes showed no interest
in prey, we lightly sedated and manually fed them using the
methods described below for the non-constricting group in order
to ensure that food intake was comparable to that of all other
individuals. For the non-constricting group, we anesthetized
each snake before each feeding using the open-drop method
(Blouin-Demers et al., 2000), which involved placing each snake
in a plastic enclosure containing a piece of tissue soaked with
1 mL Isourane anesthetic, which does not signicantly impact
metabolic rate (McCue, 2006). We left snakes in the chambers
until they rst lost the righting reex. Under this light sedation,
we manually fed each snake a whole mouse of appropriate size.
During feeding, each snake maintained strong and steady
breathing and heartbeats. We performed this procedure for
9 weeks, during which snakes gained mass but not constriction
experience. During the 10th week of feedings, non-constricting
snakes were allowed to feed and constrict their prey under normal
conditions, during which we recorded peak constriction pressures
using the methods described above.
For the experiment on experience and growth, we had two
analyses. Snakes were not signicantly different in hatchling
mass at the onset of trials. We used a two-sample t-test to test for a
difference in nal mass between the snake groups. To evaluate
peak constriction pressure at the end of the feeding trials, and to
capture variation caused by any differences in nal snake mass,
we performed an OLS regression with snake mass as the
independent variable, pressure as the dependent variable, and
treatment group as a categorical predictor. We used Past 3.08
(Hammer et al., 2001) and RStudio (version 0.99.441; RStudio
Team, 2015) for analyses and considered models signicant
whenever P<0.05. When applicable, data are presented here as
mean standard error (s.e.m.).
RESULTS
Scaling
All snakes in the scaling trials readily struck at and constricted
their prey using coils of 12 loops. In the anterior part of the coil,
the snake's ventral surface pressed against the prey, whereas in the
posterior part of most coils, the snake's body twisted such that a
lateral surface pressed against the prey (Fig. 1). Once the coil was
applied, no snake considerably readjusted its coil. Peak
constriction pressures ranged from 6.82 to 59.59 kilopascals
(kPa), which incapacitated the prey and in many cases caused
bleeding in the snout of the prey. The number of loops applied
(t¼6.4, P¼0.5; Fig. 2) and their interaction with snake diameter
(t¼1.2, P¼0.45) were not signicant factors in a full multiple-
regression model (pressure snake diameter loop number;
F
3,26
¼31.51, P<0.0001). For the nal model (pressure snake
diameter), elevation and slope did not markedly change with the
removal of outliers or high-leverage data points, so we retained
them in the analysis and gures. As snakes increased in size
(diameter), they exerted signicantly higher pressures (pressure
6.08 snake diameter 1.49; R
2
¼0.71; F
1,38
¼97.62,
P<0.0001; Fig. 2). Ball pythons exhibit differences in size, diet,
and habitat use based on their sex (Luiselli and Angelici, '98).
Despite these differences, and accounting for differences in mass
by incorporating it into the model, sex did not impact peak
constriction pressure (t¼1.4, P¼0.17; Fig. 2).
Our log-transformed slope for ball pythons (b¼1.08) was
signicantly lower than the interspecic slope from Moon and
Mehta (2007) (b¼1.39, t
38
¼2.82, P<0.005), but signicantly
higher than that from Penning et al. (2015) for two closely related
species (P. molurus bivittatus b¼0.33 and P. reticulatus b¼0.25,
t
38
¼7.57, P<0.0001 and t
38
¼6.84, P<0.0001 respectively).
Experience
Pythons in the constricting group exerted pressures of at least
4 kPa on their rst constriction attempt. For the model on nal
peak constriction pressure, nal snake mass (t¼0.51, P>0.6)
and the interaction (nal snake mass treatment; t¼0.62,
P>0.54) were not signicant factors, and were removed from the
model. Despite the increase in statistical power due to removal of
these variables, prior constriction experience did not have a
Figure 1. Juvenile ball python (Python regius, 88 cm snoutvent
length) constricting an adult mouse (Mus musculus) and
generating a peak pressure of 27.9 kPa.
J. Exp. Zool.
CONSTRICTION PERFORMANCE IN BALL PYTHONS 3
signicant effect on peak constriction pressure (constricting
group ¼12.8 1.4 kPa; non-constricting group ¼14.1 1.5
kPa; F
1,20
¼0.37, P>0.54; Fig. 3). The result is the same when
using diameter as a covariate instead of body mass (F
1,19
¼0.5,
P>0.46). Interestingly, the two groups of snakes were not
signicantly different in hatchling mass (t
20
¼1.53, P>0.14), but
snakes that constricted their prey were signicantly lighter
(75.2 2.25 g) than snakes that were not allowed to constrict
(85.2 3.3 g; t
20
¼2.45, P<0.03; Fig. 4) at the end of 10 feeding
events. These results are consistent with the high energetic cost of
constriction (Cruz-Neto et al., 2001; Canjani et al., 2003).
DISCUSSION
Ball pythons consistently constricted prey, displaying behaviors
similar to those reported for Boa constrictor (Mehta and
Burghardt, 2008), P. molurus bivittatus and P. reticulatus
(Penning et al., 2015) and other adult booids (Frazzetta, '66;
Greene and Burghardt, '78). Their stereotyped constriction differs
from the more-variable behaviors reported in Loxocemus, erycine
snakes (Mehta and Burghardt, 2008), and colubrid snakes (Mori,
'94; Mehta, 2003).
Peak constriction pressure in ball pythons depended only on
snake diameter, with larger diameter snakes exerting higher
pressures. There are several possible reasons for the differnt slope
of pressure against diameter in ball pythons than in other species
(Moon and Mehta, 2007; Penning et al., 2015). First, interspecic
scaling patterns may not reect intraspecic patterns (Penning
et al., 2015). Second, snakes may use submaximal but fully
sufcient effort in response to prey cues. For example, pressures
exerted by boas constricting sedated rats (20.79 1.99 kPa from
boas of 1.53 0.13 kg; Boback et al. 2015) are signicantly lower
than those from similarly sized ball pythons in this study
(31.42 2.52 kPa from ball pythons of 1.29 0.15 kg; t
12
¼5.1,
P<0.001). Prey movement affects constriction performance (de
Queiroz, '84; Moon, 2000; Moon and Mehta, 2007; Boback et al.,
2012) and it is possible that the lack of a struggling from sedated
prey led the boas to use submaximal constriction performance.
Ball pythons did not exert higher pressures when they used
more loops of the body, a nding similar to that of other pythons
(Penning et al., 2015) but different from interspecic observa-
tions (Moon and Mehta, 2007). Why is peak constriction pressure
unaffected by the number of loops that pythons use? Snake axial
musculature is extraordinarily complex, involving serially
repeated muscles and tendons that span multiple joints, overlap,
interconnect, and appear to act in parallel (Mosauer, '35; Gasc,
'81; Jayne '82; Moon and Gans, '98; Moon, 2000). With such
anatomy, using more of the body in a coil may add more muscles
in parallel and therefore increase force exertion. However, the
increasing surface area over which the force is applied could keep
the pressure exerted on the prey constant. Another possibility is
that variation in individual performance obscures the true
Figure 2. Peak constriction pressures measured in ball pythons of
different sizes (N¼40). The black line indicates the ordinary least-
squares regression (see Materials And Methods). The horizontal
gray bar represents the normal systolic (top of bar) and diastolic
(bottom of bar) blood pressures for Mus musculus and Rattus
norvegicus (Flindt, 2003). Pressures above the shaded bar are likely
to disrupt circulatory and brain function. The number of loops used
in the constriction coil is indicated by marker size.
Figure 3. Mean peak constriction pressures (kPa; black bars) for
snakes with no prior constriction experience (non-constricting
group; diamonds) and snakes with 9 weeks of prior constriction
experience (constricting group; triangles). Each marker represents
an individual data point.
J. Exp. Zool.
4PENNING AND DARTEZ
relationship between loop number and constriction pressure.
However, this is the third python species to display this trend:
P. molurus bivittatus (N¼17; Penning et al., 2015), P. reticulatus
(N¼48; Penning et al., 2015), and P. regius (N¼40; this study). A
third possibility is that not all loops contribute equally to pressure
exertion. The ventral and lateral bending in different parts of a
ball python's coil (Fig. 1) probably use different muscles, or
perhaps some of the same muscles but with different angles of
force exertion that would result in different degrees of force
transmission. Furthermore, using selective muscle contractions
to focus exertion on targeted areas could conserve energy, which
may be benecial because constriction is energetically expensive
(Cruz-Neto et al., 2001; Canjani et al., 2003).
The high constriction pressures exerted by ball pythons are
likely to impede circulatory function, which would impair the
prey before suffocation (McLees, '28; Hardy, '94, Moon, 2000;
Boback et al., 2015). Stopping low-pressure venous ow is
functionally equivalent to cardiac arrest because it stops all
blood ow (Parmley, '91; Moon and Mehta, 2007). A
constriction pressure of ca. 22 kPa has been shown to reduce
heart rate, increase central venous pressure, and decrease
peripheral arterial blood pressure in rats (Boback et al., 2015). In
this study, 23 of the ball pythons produced pressures similar to
or higher than the pressures shown to disrupt circulation in
prey. In ball pythons of ca. 1 m SVL, constriction pressures
exceeded systolic blood pressures in the rodents and were 50%
higher than the values shown to impede heart function (Boback
et al., 2015). The occurrence of nasal bleeding in the rodents
during many constriction events indicated that blood vessels in
the head can be ruptured during constriction, which suggests
that additional ruptures can occur elsewhere in the head.
Furthermore, pressure can travel through tissues, and neural
tissues are susceptible to pressure (Toth et al., '97; Zhang et al.,
2004; Courtney and Courtney, 2009). Some larger ball pythons
exerted pressures (4959 kPa) similar to transient pressures
(53220 kPa for 1020 ms) that can cause inju ry, neural
damage, and immediately incapacitate mammals (Toth et al.,
'97; Zhang et al., 2004; Courtney and Courtney, 2009), and
pythons can sustain their constriction pressures for several
minutes. It is likely that some constriction pressures are high
enough to not only interfere with circulatory function, but also
force blood towards the head and increase pressure in the brain
(Balldin, 02; Williams et al., 2008; Penning et al., 2015).
Unlike many young colubrid snakes (Mori, '94; Mehta, 2003),
ball pythons have sufcient constriction strength from hatching.
Ball pythons constricted with pressures of at least 4 kPa on their
rst attempt, which are probably sufcient to stop venous blood
ow in the prey (Hardy, '94; Moon, 2000). Our experiments have
shown that constriction pressures exerted by ball pythons are
high enough to kill prey by circulatory arrest and possibly by
forcing blood to the brain. Constriction strength in ball pythons is
solely dependent upon their size, and independent of the number
of loops used in a coil, sex, and their prior experience with
constriction behavior.
ACKNOWLEDGMENTS
We thank B. Clark, M. Miles, T. Lyon, and N. McCorkendale for
providing access to pythons and B. Moon for providing
equipment, reviewing and editing drafts of the manuscript, and
for fruitful discussions on constriction. We also thank P. Leberg
and J. Neigel for their contributions to the experimental design of
the experience trials and N. Haertle for his advice on snake
anesthesia. We would also like to thank C. Denesha, P. Hampton, I.
Moberly, M. Perkins, and A. Rabatsky for their helpful support,
guidance, and suggestions.
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6PENNING AND DARTEZ
... Constriction performance increases with body size both among and within species (Moon and Mehta 2007;Penning et al. 2015;Penning and Dartez 2016;Penning 2017a), although these studies found different maximum pressures and scaling exponents that warrant further study (Figs. 14.7 and 14.8). ...
... Constriction by very small snakes involves low pressures that may kill prey by suffocation (Moon and Mehta 2007). However, the constriction pressures exerted by diverse snakes are often high enough to make circulatory arrest the proximate mechanism of death in mammalian prey (Moon 2000a;Moon and Mehta 2007;Boback et al. 2015;Penning et al. 2015;Penning and Dartez 2016). Constriction may cause internal bleeding and high tissue pressures (Greene 1983;Penning and Dartez 2016), interfere with or damage neural tissue (Penning et al. 2015;Penning and Dartez 2016), and in large snakes perhaps damage the spine of a prey animal (Rivas 2004). ...
... However, the constriction pressures exerted by diverse snakes are often high enough to make circulatory arrest the proximate mechanism of death in mammalian prey (Moon 2000a;Moon and Mehta 2007;Boback et al. 2015;Penning et al. 2015;Penning and Dartez 2016). Constriction may cause internal bleeding and high tissue pressures (Greene 1983;Penning and Dartez 2016), interfere with or damage neural tissue (Penning et al. 2015;Penning and Dartez 2016), and in large snakes perhaps damage the spine of a prey animal (Rivas 2004). The dynamic and variable movements of constrictors and their prey may affect the mechanism and outcome of constriction more than the predator-prey size relationship (Moon and Mehta 2007). ...
... Constriction performance increases with body size both among and within species (Moon and Mehta 2007;Penning et al. 2015;Penning and Dartez 2016;Penning 2017a), although these studies found different maximum pressures and scaling exponents that warrant further study (Figs. 14.7 and 14.8). ...
... Constriction by very small snakes involves low pressures that may kill prey by suffocation (Moon and Mehta 2007). However, the constriction pressures exerted by diverse snakes are often high enough to make circulatory arrest the proximate mechanism of death in mammalian prey (Moon 2000a;Moon and Mehta 2007;Boback et al. 2015;Penning et al. 2015;Penning and Dartez 2016). Constriction may cause internal bleeding and high tissue pressures (Greene 1983;Penning and Dartez 2016), interfere with or damage neural tissue (Penning et al. 2015;Penning and Dartez 2016), and in large snakes perhaps damage the spine of a prey animal (Rivas 2004). ...
... However, the constriction pressures exerted by diverse snakes are often high enough to make circulatory arrest the proximate mechanism of death in mammalian prey (Moon 2000a;Moon and Mehta 2007;Boback et al. 2015;Penning et al. 2015;Penning and Dartez 2016). Constriction may cause internal bleeding and high tissue pressures (Greene 1983;Penning and Dartez 2016), interfere with or damage neural tissue (Penning et al. 2015;Penning and Dartez 2016), and in large snakes perhaps damage the spine of a prey animal (Rivas 2004). The dynamic and variable movements of constrictors and their prey may affect the mechanism and outcome of constriction more than the predator-prey size relationship (Moon and Mehta 2007). ...
Chapter
Snakes are a diverse group of squamate reptiles characterized by a unique feeding system and other traits associated with elongation and limblessness. Despite the description of transitional fossil forms, the evolution of the snake feeding system remains poorly understood, partly because only a few snakes have been studied thus far. The idea that the feeding system in most snakes is adapted for consuming relatively large prey is supported by studies on anatomy and functional morphology. Moreover, because snakes are considered to be gape-limited predators, studies of head size and shape have shed light on feeding adaptations. Studies using traditional metrics have shown differences in head size and shape between males and females in many species that are linked to differences in diet. Research that has coupled robust phylogenies with detailed morphology and morphometrics has further demonstrated the adaptive nature of head shape in snakes and revealed striking evolutionary convergences in some clades. Recent studies of snake strikes have begun to reveal surprising capacities that warrant further research. Venoms, venom glands, and venom delivery systems are proving to be more widespread and complex than previously recognized. Some venomous and many nonvenomous snakes constrict prey. Recent studies of constriction have shown previously unexpected responsiveness, strength, and the complex and diverse mechanisms that incapacitate or kill prey. Mechanisms of drinking have proven difficult to resolve, although a new mechanism was proposed recently. Finally, although considerable research has focused on the energetics of digestion, much less is known about the energetics of striking and handling prey. A wide range of research on these and other topics has shown that snakes are a rich group for studying form, function, behavior, ecology, and evolution.
... 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. ...
... 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. ...
... 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 a priori how the surface area of contact should change with size during the dynamic interaction between predator and prey (Penning et al., 2015). ...
Article
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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 maximumpulling 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 superior constriction 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.
... Constriction is a behavioral pattern that immobilizes prey with two or more points on the snake's body (Greene & Burghardt, 1978), typically involving fully encircling body loops around the prey (Mehta, 2003;Moon & Mehta, 2007;Penning, Dartez & Moon, 2015). Constriction behavior is a key innovation in the evolution and radiation of snakes (Greene & Burghardt, 1978;Lillywhite, 2014), is integral to their feeding biology (Moon, 2000), and is therefore an evolutionarily and functionally important predation mechanism (Greene & Burghardt, 1978;Penning & Dartez, 2016). ...
... However, to my knowledge, the functional limitations of constriction on small prey have not been tested. Constriction is an energetically expensive behavior (Canjani et al., 2003;Penning & Dartez, 2016) and snakes can modulate their efforts in response to prey cues (Moon, 2000;Boback et al., 2012), so seizing and eating small prey alive likely reduces the energy demands on the snake without high risks of injury from small prey. While smaller prey may be eaten alive, larger and more active prey are typically constricted (de Queiroz, 1984;Mehta, 2003Mehta, , 2009Penning & Cairns, 2016). ...
... cm). Maximum body diameters (the primary predictor of constriction performance; Moon & Mehta, 2007;Penning et al., 2015;Penning & Dartez, 2016) varied by less than 2 cm. All snakes were at least 2 years old and the sample consisted largely of one sex (19 females, 1 male). ...
Article
Full-text available
Constriction is an evolutionarily and functionally important behavior that many snakes use to subdue a variety of prey. However, little work has examined the effects of prey size on constriction performance. Furthermore, many snakes are known to feed even while previously consumed prey remain in the stomach. This temporary increase in mass may place constraints on subsequent performance. To test these effects, I investigated constriction performance in eastern kingsnakes Lampropeltis getula handling different sizes and quantities of rodent prey in two experiments by measuring coil length and peak constriction pressure. In the first experiment, constriction coil length and peak constriction pressure did not differ significantly between snakes feeding on either ‘small’ (5% relative prey mass, RPM) or ‘large’ (15% RPM) rodent prey. However, there was a significant interaction between prey size and repeated feeding. Snakes that had previously consumed large meals had significantly shorter coil lengths and lower peak constriction pressures when fed for a second time (reductions of 60 and 51%, respectively). In Experiment 2, snakes offered five sequential, similarly sized prey (@ 7% RPM), showed a regular decrease in coil length and peak constriction pressure across sequential feeding trials. During the final (fifth) trials, snakes used 45.7% shorter coils and exerted 50.1% lower peak constriction pressures. Thus, prey size alone did not affect constriction performance, but predation performance was significantly affected by the prior consumption of prey ≥7% RPM, and performance was further reduced during additional feeding trials.
... Previously, these individuals have demonstrated levels of strike performance that matched those of other snake species measured (Ryerson and Tan, 2017). Ball pythons are able to increase constriction pressure with size, a result of increasing axial musculature (Penning and Dartez, 2016), and I predict strike performance will also be maintained throughout ontogeny, similarly to patterns to patterns in Trimeresurus (Herrel et al., 2011). Ball pythons are known to be sexually dimorphic (Luiselli and Angelici, 1998), but there is little evidence of male-male combat or other areas where performance may be impacted by SSD (Luiselli and Angelici, 1998), and so I predict that there will no differences between males and females. ...
... Snakes were fed a previously killed mouse once every two weeks. Prey size was increased along with body mass of the snakes to maintain an approximate prey size of 10%, following Penning and Dartez (2016). Snakes switched from mice to small rats to accommodate the increase in body size. ...
Article
The rapid strike of snakes has long been of interest in terms of mechanical performance. Recently, several nonvenomous taxa have been found to strike with the same incredible strike velocity and acceleration as the high-performing vipers. However, little is known regarding how these patterns change through ontogeny. Here I present ontogenetic strike data on ten ball pythons (Python regius) over a three year time period, from birth to sexual maturity. I found that performance declined rapidly over the first 18 months in nearly all kinematic measures. This puts the adult data out of the currently developing trend of high performance being maintained across the diversity of snakes. The underlying cause of the decline in performance is unclear, but there are several avenues of behavior, morphology, biomechanics, and ecology to be investigated.
... Ball pythons are completely terrestrial ambush predators, who also use constriction to subdue their prey. The feeding performance of both species is quite similar, they strike with similar mechanics (Ryerson and Tan, 2017;Ryerson and Van Valkenburg, 2021) and generate high pressures when constricting (Boback et al., 2015;Penning and Dartez, 2016). Ball pythons have not been observed to feed in an arboreal context, although stomach contents regularly contain birds and males have been observed climbing in trees (Luiselli and Angelici, 1998). ...
Article
Snakes are a diverse group of reptiles, having colonized almost every environment on the planet. Multiple snake lineages have independently evolved semiarboreal or completely arboreal species. As snakes lack limbs, the challenges of moving and feeding in an arboreal environment are numerous. Here we compare the prey-handling ability of the semiarboreal boa constrictor to the terrestrial ball python in a simulated arboreal context. Snakes were allowed to strike at rodent prey and attempt to swallow that prey while suspended. Boa constrictors were successful in feeding, using a complex suite of behaviors to maintain their position and manipulate their prey. Boa constrictors positioned rats so that swallowing occurred in the direction of gravity, and would use loops of their body to support the rat during swallowing. Ball pythons were frequently not successful in feeding, lacking the complex behaviors that boa constrictors frequently employed. Ball pythons would attempt to swallow, but in the majority of feeding attempts were ultimately unsuccessful. These unsuccessful feeding attempts were typically characterized by the ball pythons hanging upside-down, trying to swallow the prey against the direction of gravity. We suggest that behavioral modifications to feeding encouraged successful invasion of arboreal habitats, but more sampling of snake diversity is needed to explore the range and types of feeding behaviors that arboreal snakes employ.
Article
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Across the diversity of vertebrates, bite force has been studied and suggested to have important ecological and evolutionary consequences. However, there is a notable lineage of vertebrates that use this performance trait yet are missing from the bite-force literature: the snakes. Snakes often rely on biting during prey subjugation and handling. Many snakes bite and hold prey while a constriction coil is formed or while venom is being delivered, or both. Others use biting exclusively without employing any additional prey-handling behaviors. In addition to biting, constriction is an important predation mechanism. Here, I quantify bite force and constriction pressure in kingsnakes (Lampropeltis getula). Furthermore, I explore the proximate determinants of bite force as well as the relationship between biting and constriction performance. Bite force increased linearly with all head and body measures. Of these, head height was the best predictor of bite force. Bite force in kingsnakes was within the range of values reported for lizards, but their relative performance was lower for their head size compared to lizards. Peak constriction pressure also increased with all body measures. Biting and constricting use 2 different parts of the musculoskeletal system and are positively and significantly correlated with one another. Future work targeting a greater diversity of snakes that rely more heavily on biting may reveal a greater range of bite performance in this diverse and successful vertebrate group. © 2016 International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd
Article
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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 Schneider 1801 and Python molurus bivittatus Kuhl 1820) 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.
Article
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As legless predators, snakes are unique in their ability to immobilize and kill their prey through the process of constriction, and yet how this pressure incapacitates and ultimately kills the prey remains unknown. In this study, we examined the cardiovascular function of anesthetized rats before, during and after being constricted by boas (Boa constrictor) to examine the effect of constriction on the prey's circulatory function. The results demonstrate that within 6 s of being constricted, peripheral arterial blood pressure (PBP) at the femoral artery dropped to 1/2 of baseline values while central venous pressure (CVP) increased 6-fold from baseline during the same time. Electrocardiographic recordings from the anesthetized rat's heart revealed profound bradycardia as heart rate (fH) dropped to nearly half of baseline within 60 s of being constricted, and QRS duration nearly doubled over the same time period. By the end of constriction (mean 6.5±1 min), rat PBP dropped 2.9-fold, fH dropped 3.9-fold, systemic perfusion pressure (SPP=PBP-CVP) dropped 5.7-fold, and 91% of rats (10 of 11) had evidence of cardiac electrical dysfunction. Blood drawn immediately after constriction revealed that, relative to baseline, rats were hyperkalemic (serum potassium levels nearly doubled) and acidotic (blood pH dropped from 7.4 to 7.0). These results are the first to document the physiological response of prey to constriction and support the hypothesis that snake constriction induces rapid prey death due to circulatory arrest. © 2015. Published by The Company of Biologists Ltd.
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For most vertebrates, locomotor activity begins at the time of hatching or birth. Although handicapped by small size, rapidly growing tissues, and naïveté, juveniles of most species must maneuver in the same environment and avoid the same predators as adults. Thus, it is not surprising that some ectothermic and precocial endothermic tetrapods undergo ontogenetic changes that allow juveniles to sprint almost as fast and jump almost as far as adults. Allometric changes that have been shown or suggested to enhance performance in juveniles include relatively longer limbs, relatively greater muscular forces and contractile velocities, and higher muscular mechanical advantage. Compensation for rapid growth has been shown to occur in the bones of precocial birds and mammals. The limb bones of these animals have relatively greater cross-sectional diameters and areas than those of adults. This maintains a parity of bone and muscular strength during periods of rapid growth, when bones are composed of weaker, more flexible tissue. In contrast to their sprinting and jumping performance, young animals appear to have significantly less locomotor stamina and agility than adults. The lower stamina may, in large part, simply be a consequence of juveniles being smaller than their parents. The awkwardness of youth appears to result from a conflict between the process of growth and the effective integration of the sensory, neural control, and motor systems. Because juveniles often suffer higher rates of mortality from predation, selection for improved locomotor performance is likely to be strong. Consequently, as a possible result of ontogenetic canalization, the adult phenotype may be determined as much or more by selection on the locomotor performance of juveniles as by direct selection on the locomotor abilities of adults.
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A comprehensive, but simple-to-use software package for executing a range of standard numerical analysis and operations used in quantitative paleontology has been developed. The program, called PAST (PAleontological STatistics), runs on standard Windows computers and is available free of charge. PAST integrates spreadsheettype data entry with univariate and multivariate statistics, curve fitting, time-series analysis, data plotting, and simple phylogenetic analysis. Many of the functions are specific to paleontology and ecology, and these functions are not found in standard, more extensive, statistical packages. PAST also includes fourteen case studies (data files and exercises) illustrating use of the program for paleontological problems, making it a complete educational package for courses in quantitative methods.
Article
Food habits of the royal python (Python regius) were studied in some localities of southeastern Nigeria by means both of faeces analysis and forced regurgitation of living individuals. Female pythons were significantly longer than the males. Both sexes preyed exclusively upon birds and mammals, but there were significant intersexual differences in terms of dietary, composition. Males preyed more frequently upon birds (70.2% of the total number of prey items) whereas females preyed more frequently upon mammals (66.7% of the total number of prey items). There was an apparent ontogenetic change in the diet of both sexes: specimens shorter than 70 cm total length preyed almost exclusively upon small sized birds (nestlings and immature), whereas the longer specimens (> 100 cm total length) preyed almost entirely upon small mammals. We suggest that the two sexes are different in terms of their main natural history traits (males being more arboreal than females), and that this behavioural difference can explain the observed intersexual differences in dietary composition.