Blackwell Publishing LtdOxford, UKBIJBiological Journal of the Linnean Society0024-40662007 The Linnean Society of London? 2007
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Original Articles
LEGLESS LIZARD FEEDING BEHAVIOUR
M. WALL and R. SHINE
Biological Journal of the Linnean Society, 2007, 91, 719–727. With 5 figures
Dangerous food: lacking venom and constriction, how do
snake-like lizards (Lialis burtonis, Pygopodidae) subdue
their lizard prey?
MICHAEL WALL* and RICHARD SHINE
Biological Sciences A08, University of Sydney, NSW 2006 Australia
Received 22 November 2005; accepted for 20 November 2006
Snakes are renowned for their ability to subdue and swallow large, often dangerous prey animals. Numerous adaptations, including constriction, venom, and a strike-and-release feeding strategy, help them avoid injury during predatory encounters. Burton’s legless lizard (Lialis burtonis Gray, Pygopodidae) has converged strongly on snakes. It is
functionally limbless and feeds at infrequent intervals on relatively large prey items (other lizards) capable of inflicting a damaging bite. However, L. burtonis possesses neither venom glands, nor the ability to constrict prey. We investigated how L. burtonis subdues its prey without suffering serious retaliatory bites. Experiments showed that lizards
modified their strike precision according to prey size; very large prey were always struck on the head or neck, preventing them from biting. In addition, L. burtonis delayed swallowing large lizards until they were incapacitated,
whereas smaller prey were usually swallowed while still struggling. Lialis burtonis also displays morphological
adaptations protecting it from prey retaliation. Its long snout prevents prey from biting, and it can retract its lidless
eyes out of harm’s way while holding onto a food item. The present study further clarifies the remarkable convergence between snakes and L. burtonis, and highlights the importance of prey retaliatory potential in predator
evolution. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 719–727.
ADDITIONAL KEYWORDS: evolution – foraging ecology – predator–prey interactions – squamate reptiles.
INTRODUCTION
Predators often expose themselves to significant risk
when capturing and subduing prey items. Selection
pressure for prey to retaliate is strong (Dawkins &
Krebs, 1979), and many species may do so effectively.
For example, prey animals are known to inflict serious
or even fatal injuries on predators, ranging from lions
and tigers (Schaller, 1967, 1972) to birds (Morejohn,
1969; Mock & Mock, 1980), snakes (Fleay, 1981; Webb
& Shine, 1993a), fishes (Rubinoff & Kropach, 1970;
Wanjala & Tash, 1983), spiders (Edmunds, 1974),
insects (Lucas & Brockmann, 1981), and gastropods
(Dietl, 2003).
Thus, counter-selection acts powerfully on predators
that prey upon potentially dangerous animals, working to minimize their risks (Brodie & Brodie, 1999).
For example, jumping spiders that specialize on ants
*Corresponding author. E-mail: [email protected]
often back away after inflicting a bite, only moving in
again once their venom has immobilized the victim
(Jackson & van Olphen, 1992; Pekar, 2004). Whereas
whiptail lizards (Aspidoscelis gularis) simply seize
and swallow innocuous crickets, they aggressively
shake and throw scorpions (O’Connell & Formanowicz, 1998). Grasshopper mice (Onychomys torridus)
push the abdomens of beetles ( Eleodes, Chlaenius)
into the ground before the insects have a chance to
spray their noxious chemical cocktail (Eisner & Meinwold, 1966). Such adaptive responses need not be
solely behavioural. For example, a toxicological arms
race is ongoing between garter snakes ( Thamnophis
sirtalis) and their newt prey (Taricha); as the newts
become more toxic, the snakes become more resistant
(Brodie & Brodie, 1999; Brodie et al., 2005).
One group of animals that deals regularly with
potentially dangerous prey is snakes. In general,
snakes feed at infrequent intervals and take relatively large prey, a foraging strategy that was likely
a key innovation in their impressive adaptive radia-
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 719–727
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M. WALL and R. SHINE
tion (Greene, 1983). Snakes famously display a suite
of morphological adaptations effecting dramatic cranial kinesis, their flexible skulls facilitating ingestion
of bulky prey items whole (Greene, 1997). Although
swallowing large, powerful prey animals poses a
serious challenge, subduing them without incurring
injury is at least as important, and snakes have
evolved several specializations to this end. With a
few exceptions (e.g. coachwhips, Masticophis flagellum, simply pinioning and swallowing rodents;
Werler & Dixon, 2000), snakes utilize constriction or
venom, or both, to immobilize and incapacitate dangerous prey that may outweigh them by up to 50%
(Greene, 1983, 1997; Shine & Schwaner, 1985).
Although venom may be ancestral in advanced
snakes, sophisticated front-fanged venom delivery
systems have evolved multiple times in this group
(Fry et al., 2003) and are often associated with the
ability to take especially large prey (e.g. in vipers;
Greene, 1997).
Snakes also exhibit behavioural adaptations that
minimize their risks in predatory encounters. For
example, venomous species of multiple lineages strike
and release rodents to avoid a damaging retaliatory
bite; they then trail and consume their prey after it
has succumbed (Allon & Kochva, 1974; Johnson, 1975;
Kardong, 1982; Shine & Covacevich, 1983; Witten,
1985; Kardong & Smith, 2002; Greenbaum, 2004).
By contrast, smaller, more innocuous prey animals,
such as frogs and insects, are often simply held and
swallowed (Allon & Kochva, 1974; Kardong, 1982;
Witten, 1985; Shine, 1991; Greenbaum, 2004).
What happens when a species converges on snakes
ecologically but is phylogenetically constrained from
utilizing their most effective weaponry? The Australian pygopodid Burton’s legless lizard (Lialis burtonis) offers the opportunity to answer this question.
Like snakes, L. burtonis is functionally limbless and
feeds infrequently on relatively large prey items
(primarily scincid lizards), which it takes from
ambush (Patchell & Shine, 1986a; Murray, Bradshaw
& Edward, 1991). Lialis burtonis stomachs contain
food only 21–33% of the time (Huey, Pianka & Vitt,
2001; Wall, 2006), and individuals are capable of subduing and swallowing whole prey animals at least
45% of their own mass (M. Wall, pers. observ.). Prey
lizards this large are capable of inflicting a damaging
bite. For example, Egernia whitii, a species consumed
by L. burtonis in the laboratory (M. Wall, pers.
observ.), bites with 18.5 N of force (Langkilde, 2005),
harder than some turtles (Herrel, O’Reilly & Richmond, 2002).
Unlike snakes that take large prey, however,
L. burtonis has no obvious, dramatic armaments at
its disposal; as a descendant of geckos (Kluge, 1976;
Donnellan, Hutchinson & Saint, 1999), it possesses
neither venom glands, nor constricting ability.
Indeed, the other 40 or so pygopodid species (with
the exception of a congener, Lialis jicari) retain the
arthropod diet of their gecko ancestors (Cogger,
2000). Other studies of L. burtonis (Patchell & Shine,
1986a, b, c) have noted its convergence with snakes
but have focused primarily on the parallel morphological adaptations that allow it to swallow such large
meals (e.g. a highly kinetic skull). How it subdues its
struggling, often powerful prey without sustaining
serious injury has not been explored. How does
L. burtonis solve a problem that snakes have
addressed with such substantial measures as venom
and constriction?
We set out to answer this question by staging
encounters in the laboratory between L. burtonis and
prey animals of varying sizes (and thus varying retaliatory potentials). We hypothesized that L. burtonis
would exhibit behavioural adaptations minimizing the
risk of injury from dangerous prey. Specifically, we
predicted that, when dealing with large prey items,
the lizard would modify: (1) its strike accuracy, (2) the
distance from which its strike is launched, and (3) its
preparedness to swallow still-struggling prey. Furthermore, we also expected to document morphological adaptations preventing prey retaliation or
reducing its effects (e.g. some means of protecting vulnerable parts of the anatomy such as the eye). The
present study was designed to shed further light on
the nature of the convergence between L. burtonis and
snakes, as well as to clarify the selective pressures
that potentially dangerous prey items may impose on
their predators.
MATERIAL AND METHODS
STUDY
ANIMALS AND MAINTENANCE
In March 2003, 17 adult L. burtonis [five males, 12
females; mean snout–vent length (SVL) = 19.31
± 0.53 cm; mean mass = 15.76 ± 1.49 g] were captured
in Australia’s tropical Northern Territory, approximately 50 km south-east of Darwin. Lizards were
brought to the University of Sydney, where they were
maintained individually in plastic cages (22 × 22 ×
7.5 cm) on a 12 : 12 h light/dark cycle and fed live
skinks approximately biweekly. Room temperature
was kept at 20 °C, but heated strips (approximately
39 °C) running under one end of each cage allowed
lizards to thermoregulate behaviourally during the
diurnal part of their daily cycle. They also had access
to shelter and water ad libitum. All animals were collected with the permission of the Parks and Wildlife
Commission of the Northern Territory, and all activities were undertaken with the permission of the animal ethics committee at the University of Sydney
(approval number L04/5-2002/3/3563).
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 719–727
LEGLESS LIZARD FEEDING BEHAVIOUR
EXPERIMENTAL
PROTOCOLS
Behavioural adaptations
We videotaped feeding trials of each L. burtonis
with four different, non-overlapping size classes of
prey: 0.051 ± 0.001 relative prey mass (RPM; prey
mass = 5.1% of predator mass), 0.128 ± 0.003 RPM,
0.269 ± 0.006 RPM, and 0.413 ± 0.004 RPM (hereafter
0.05, 0.13, 0.27, and 0.41 RPM). We could thus gauge
the responses of lizards to prey of varying retaliatory
potential, from innocuous (0.05 RPM) to dangerous
(0.41 RPM). Because a wide range of RPMs was
required, prey items consisted of locally caught scincid
lizards of various species. All skinks used shared a
similar, robust-limbed body plan; no limb-reduced burrowers were employed. Prey lizards were presented
sequentially, in random order. Lialis burtonis were
always given at least 3 weeks between trials to ensure
hunger and motivation to feed. As L. burtonis prey
predominantly upon diurnal skinks (Patchell & Shine,
1986b), trials always took place between 10.00 h and
16.00 h, from August 2004 to April 2005.
One hour before each trial began, a single
L. burtonis was moved from its home cage into a different room set at 25 °C and placed in a 45-L test
arena (49 × 35 × 30 cm). White paper lined the bottom
and sides of the arena, and a 5-cm scale drawn on the
paper provided a distance reference. One hour later, a
live skink was dropped into the arena 20 cm from the
snout of the L. burtonis, at which time videorecording
commenced and the experimenter left the room. A different, clean arena was used for each trial, and only
one L. burtonis was tested at any one time.
A variety of relevant variables were scored from the
videotape, including the location and distance of the
first strike to hit the prey item, whether or not prey bit
L. burtonis during the predatory episode, and whether
or not prey items were swallowed prior to being fully
subdued (i.e. still struggling). For strike location, all
strikes were assigned to one of four sites: head/neck
(anywhere anterior to the pectoral girdle); chest (from
the pectoral girdle posteriad to midway between the
pectoral and pelvic girdles); abdomen (from below the
pectoral-pelvic girdle midpoint posteriad to the vent);
and tail. In addition, we performed an experiment
designed to determine how strike location affected the
ability of prey lizards to retaliate. We gripped 19 adult
male water skinks (Eulamprus heatwolei), a species
L. burtonis consumes in the laboratory (M. Wall, pers.
observ.), at the pectoral girdle with a pair of forceps for
60 s. We scored whether skinks were able to: (1) turn
and bite; and (2) wriggle free and escape. Nineteen different adult male E. heatwolei were then held at the
pelvic girdle, and the same information was recorded.
Constant and equal pressure was maintained via the
forceps in all trials. Continuous data were log-
721
transformed to ensure normality and homogeneity of
variances.
Morphological adaptations
The snout of Lialis burtonis is exceptionally long and
attenuated, dramatically different from that of any
other lizard or snake found in Australia. An experiment was performed to determine whether this shape
reduces the probability of receiving a retaliatory bite
from a food item. We held 19 adult male E. heatwolei
fully across the pectoral girdle with forceps for 60 s,
again scoring whether or not skinks bit or escaped.
Then, 19 different adult male E. heatwolei were held
60% of the way across the pectoral girdle (simulating
the grip maintained by predators with shorter snouts,
such as sympatric elapid snakes), and these same
variables were scored. Again, constant and equal pressure was applied in each trial.
During the course of previous studies, we noticed
that L. burtonis is able to partially retract its eyes in
response to an actual or impending touch. Another
experiment was therefore performed, testing the
hypothesis that this ability serves to protect the
lizard’s eyes from the thrashings of a prey item.
Eleven L. burtonis (two males, nine females; mean
SVL = 19.55 ± 0.61 cm; mean mass = 15.28 ± 1.29 g)
were fed one live skink each. When a skink was in the
predator’s jaws, we dragged the foot of another skink
across the eye of each L. burtonis to simulate the
struggling of a prey animal; we then recorded whether
or not the eye was retracted.
RESULTS
BEHAVIOURAL
ADAPTATIONS
Strike accuracy and its consequences
Lialis burtonis nearly always struck prey of all sizes
on the chest, head, or neck; strikes to the abdomen and
tail were rare (Fig. 1). However, at the largest prey
size (0.41 RPM), every strike was directed to the head
or neck (Fig. 1). When strike location was translated
into a continuous variable, expressed as a proportion
of the distance from the prey’s snout to its vent, this
difference was found to be significant [repeated
measures analysis of variance (ANOVA): F16,3 = 3.74;
P = 0.017]. Post-hoc tests revealed that prey in the
0.41 RPM class were struck significantly closer to the
head than were smaller (0.05, 0.13, and 0.27 RPM)
prey (Fisher’s PLSD; P < 0.05 in all cases; Fig. 1).
Prey rarely managed to land a retaliatory bite on
L. burtonis; such bites were observed in only two of 68
feeding trials, once each at 0.05 RPM and 0.13 RPM.
In the forceps trials, strike location had a significant
effect on the ability of E. heatwolei to deliver a retaliatory bite: 15 of 19 lizards held at the pelvic girdle
bit the forceps, whereas none did when held at the
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 719–727
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M. WALL and R. SHINE
20
20
0.05 RPM
0.13 RPM
0.41 RPM
10
Number of lizards
Number of lizards
15
0.27 RPM
15
Prey Not Subdued
10
Prey Subdued
5
5
0
0.05
0.13
0.27
0.41
Prey size (RPM)
0
Head
Chest
Abdomen
Tail
Strike Location
Figure 1. Location of Lialis burtonis feeding strikes
directed at prey skinks of varying sizes (relative prey mass,
RPMs). The first strikes to hit skinks were scored. Head,
head or neck of prey (anywhere anterior to the pectoral
girdle); Chest, from the pectoral girdle posteriad to the
midpoint between the front and rear legs; Abdomen, from
the midpoint between the front and rear legs posteriad to
the vent; Tail, anywhere posterior to the vent. For details
of statistical analysis, see text.
pectoral girdle (χ2 = 24.78, d.f. = 1, P < 0.0001). No
E. heatwolei escaped in either condition.
Strike distance
At 0.05 RPM, L. burtonis struck prey from
26.7 ± 3.9 mm away; at 0.13 RPM from 25.4 ± 3.3 mm;
at 0.27 RPM from 37.7 ± 4.7 mm; and at 0.41 RPM
from 25.2 ± 3.2 mm. These values did not differ significantly (repeated measures ANOVA: F16,3 = 1.62;
P = 0.20).
Cues for swallowing
Lialis burtonis delayed swallowing large prey until
the food item had ceased struggling, whereas smaller
lizards were often consumed while still resisting
(logistic regression, χ2 = 33.09, d.f. = 3, P < 0.0001;
Fig. 2). For example, at 0.05 RPM, 15 of 17 skinks
were still struggling when swallowed, compared to
only one of 17 at 0.41 RPM (Fig. 2). It should be noted
that because these data are not independent, they violate one of the assumptions of logistic regression.
However, any confounding effects of non-independence would likely cancel out, as each L. burtonis was
subjected to each treatment equally (Quinn & Keough,
2002). Furthermore, the result remains significant
even if α is arbitrarily lowered to 0.0001 to account for
this issue.
Figure 2. Whether or not Lialis burtonis subdued prey
prior to commencing ingestion, as a function of relative
prey mass (RPM). A prey animal was regarded as subdued
if it was not struggling overtly when swallowed. For details
of statistical analysis, see text.
MORPHOLOGICAL
ADAPTATIONS
Preventing prey retaliation
Five of 19 E. heatwolei turned and bit the forceps
when gripped across 60% of the width of the chest;
none did so when held all the way across the chest
(χ2 = 5.76, d.f. = 1, P = 0.016; Fig. 3A). Similarly, 12 of
19 skinks escaped when held across 60% of the chest,
compared to zero in those that were gripped across the
full width of the pectoral girdle (χ2 = 17.54, d.f. = 1,
P < 0.0001; Fig. 3B).
Protecting vulnerable parts of the anatomy
All 11 L. burtonis retracted their eyes (Fig. 4) upon the
touch of a skink foot.
DISCUSSION
Snake evolution has been strongly influenced by the
ability of prey to retaliate. For example, the glossy
scales, infrequent ‘binge’ feeding habits, and camouflaging chemical secretions of blindsnakes and threadsnakes serve both to limit their exposure to biting,
stinging ant prey and to reduce the damage from
retaliatory attacks (Punzo, 1974; Webb & Shine,
1993b; Kley & Brainerd, 1999; Webb, Branch & Shine,
2001). Constriction, venom, and strike-and-release
foraging are all adaptations allowing more advanced
serpents to minimize the risks incurred when taking
dangerous prey items such as rodents (Kardong, 1986;
Greene, 1997). Our data show that the snake analogue
L. burtonis, which lacks venom glands and the ability
to constrict prey, has evolved parallel strategies for
feeding upon large lizards capable of inflicting a damaging bite.
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 719–727
LEGLESS LIZARD FEEDING BEHAVIOUR
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A
Number of skinks
20
15
Skink didn't bite
10
Skink bit
5
0
Entire
60%
Grip across chest
B
Number of skinks
20
15
Skink didn't escape
10
Skink escaped
Figure 4. Photographs showing one Lialis burtonis with
its eye exposed (top) and retracted (bottom). The white
object in the bottom photo is the swab used to induce
retraction.
5
0
Entire
60%
Grip across chest
Figure 3. Frequency of biting (A) and escaping (B) by scincid lizards (Eulamprus heatwolei) when held by forceps in
one of two conditions: fully across the chest (from the left
front leg to the right) and 60% across the width of the chest.
For details of statistical analysis, see text.
First, L. burtonis modifies several aspects of its
predatory behaviour when dealing with large, potentially dangerous prey items. For example, lizards
increase their strike accuracy and precision, directing
strikes exclusively to the head and neck of exceptionally large prey. This precision, which L. burtonis
achieves without a reduction in strike distance, helps
lizards to stay out of harm’s way; prey skinks grabbed
at the pelvic girdle are capable of turning and delivering a bite, whereas those held at the chest or above
are not. Indeed, after being seized, skinks almost
never bit L. burtonis.
Skinks grabbed at the pectoral girdle are incapable
of biting back, so why do L. burtonis strike the very
largest prey exclusively more anteriad, at the head
and neck? There are several possible reasons. First,
L. burtonis may simply be playing safe; if a skink were
to lunge forward suddenly, a strike directed at its head
or neck would likely hit its chest, still preventing a
retaliatory bite. However, a strike aimed at the pectoral girdle in such a situation could land on the abdomen, allowing the skink to turn and bite. Second,
L. burtonis may be able to maintain its hold on very
large skinks only at the head or neck, regions which
are relatively narrow (Fig. 5). A very large skink
seized at the pectoral girdle may simply be too wide for
the jaws of L. burtonis, and may thus be able to break
free and/or deliver a damaging bite. Analogously, birds
struck on the head by Shedao pit-vipers (Gloydius
shedaoensis) escape less frequently than do those hit
on the body (Shine et al., 2002). Moreover, even if
L. burtonis is able to hold onto large skinks struck at
the chest, it may have trouble subduing them. Lialis
burtonis subdues food items by applying pressure with
its jaws until prey succumb to asphyxiation or exhaustion (Patchell & Shine, 1986a). This may be impossible
or inordinately difficult to achieve when large prey
animals are held by the relatively wide, strongly
reinforced chest. As L. burtonis usually attempts to
incapacitate prey lizards by squeezing at the strike
location (except on the rare occasions when strikes
land at less vulnerable sites such as the abdomen or
tail; M. Wall, pers. observ.), ease of incapacitation may
indeed be a reason to increase strike precision with
large prey.
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 719–727
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M. WALL and R. SHINE
A
Prey width (cm)
15
10
5
0
0.00
0.10
0.20
0.30
0.40
0.50
Prey size (RPM)
B
Skink width (cm)
10
9
8
7
6
Head
Neck
Chest
Location
Figure 5. A, increase of body width with relative prey
mass (RPM) in all prey skinks used in the feeding trials.
Body width was measured at the skinks’ widest point.
Points are means ± standard error (SE). Differences were
significant [analysis of variance (ANOVA); F3,64 = 56.50;
P < 0.0001). Post-hoc tests (Fisher’s PLSD) revealed significant differences between all combinations (P < 0.0005 in all
cases). B, widths at various locations on the bodies of ten
coppertail skinks (Ctenotus taeniolatus), one species used
in the feeding trials. Points are means ± SE. Differences
were significant: (repeated measures ANOVA; F9,2 = 96.14;
P < 0.0001). Post-hoc tests (Fisher’s PLSD) revealed significant differences between all combinations (P < 0.0001 in all
cases).
Similarly, some snakes taking large, dangerous prey
also employ precision striking to reduce the risk of
injury. Even venomous species that release prey a
fraction of a second after the bite may target specific
areas on a victim’s body. For example, multiple species
of pit-viper most often strike rodents on the head or
thorax (Kardong, 1986; Barr, Wieburg & Kardong,
1988; Schmidt, Hayes & Hayes, 1993). As with
L. burtonis, such precision functions in both offensive
and defensive capacities; prey struck at these sites not
only die quickly, but also are unable to inflict a retaliatory bite (Kardong, 1986).
Lialis burtonis also modifies its poststrike behaviour when dealing with very large prey. Lizards took
the time and effort to incapacitate larger skinks,
whereas smaller ones were more often swallowed
while still struggling. Such context-dependent prey
subdual minimizes both the risk of injury from large
prey and the energy expended on innocuous food
items. Again, a similar pattern is seen in some snakes,
even those with venom or constriction at their disposal. For example, northern Pacific rattlesnakes
(Crotalus oreganus) and Malay pit-vipers (Calloselasma rhodostoma) release large mice after a predatory strike but often retain smaller individuals in
their jaws (Kardong, 1986; Barr et al., 1988).
Lialis burtonis exhibits morphological adaptations
protecting it from large, potentially dangerous prey as
well. Although admittedly crude, the second forceps
experiment demonstrated that the lizard’s long snout
helps it maintain a secure grip on food items, preventing skinks from turning and biting or escaping.
Furthermore, an elongate, attenuate snout likely
enhances vision by increasing binocular overlap
(Henderson & Binder, 1980); thus, the shape of its
skull may prevent prey retaliation in an indirect manner as well, enabling L. burtonis to direct its feeding
strikes more precisely. Other aspects of the skull morphology of L. burtonis also serve to reduce its risk of
injury from struggling prey. The pointed, hinged,
recurved teeth of L. burtonis facilitate a tight grip on
slippery skinks, and its flexible mesokinetic and hypokinetic joints allow the tips of the snout to come in
contact around a prey item, effectively encircling it
(Patchell & Shine, 1986a, c).
The skull musculature of L. burtonis is also highly
specialized. First, the skull is more elongate than in
other lizards and snakes of similar size: postocular
skull elongation permits more room for jaw adducting
musculature and increases the angle through which it
inserts, imparting a more mechanically advantageous
bite (Patchell & Shine, 1986a). Second, the jaw muscles of L. burtonis are evidently highly resistant to
exhaustion. Skinks in the 0.41 RPM size class ceased
struggling after an average of 20.1 min, with some
requiring up to 48.5 min of sustained jaw pressure
before being incapacitated. In no feeding trial did a
L. burtonis visibly tire or loosen its grip. We did not
measure metabolic rates during prey subdual episodes, so we cannot say how energetically costly this
activity is to L. burtonis; it must, however, require a
great deal of muscular endurance. By comparison,
constriction of prey by snakes often takes considerably
less time (Moon, 2000; Canjani et al., 2002) but still
raises metabolic rates above those experienced during
strenuous locomotion (Canjani et al., 2002). Snakes
tend to apply force only intermittently during constriction (Moon, 2000), probably to minimize such
energetic costs, prevent muscular exhaustion, and/or
reduce lactic acid build-up. Lialis burtonis appears to
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 719–727
LEGLESS LIZARD FEEDING BEHAVIOUR
be taking analogous measures. When subduing prey
items, it maintains a baseline level of pressure; however, it also contracts its jaw muscles spasmodically
and intermittently (Murray et al., 1991; M. Wall, pers.
observ.), often in response to prey movement (as occurs
in constricting snakes; Moon, 2000).
The retractable eye of L. burtonis constitutes
another morphological adaptation minimizing risks
when dealing with dangerous prey. At a touch, or
merely the threat of a touch, the lizard can withdraw
its eyes both inward (toward the brain) and backward
(toward the ear). When viewed from above, the
retracted eye is obscured (and protected) by a protruding brow ridge (M. Wall, pers. observ.). Our data show
that lizards employ this capability during encounters
with prey; all L. burtonis retracted their eyes upon the
experimentally administered touch of a skink foot, a
rough but reasonable approximation of a struggling
prey item.
Eye retraction is likely of key importance to
L. burtonis. Like most other ambush-foraging lizards
and snakes (Greene, 1997; Pianka & Vitt, 2003),
L. burtonis is a visually orientated predator. It cues its
strikes on prey movement and does not noticeably
respond to prey scent (Wall, 2006). Its precision feeding strikes probably require uncompromised visual
input from both eyes, so any ocular damage would
likely incur serious fitness consequences. Furthermore, because it is descended from geckos (Kluge,
1976; Donnellan et al., 1999), L. burtonis cannot simply shut its eyes when prey are flailing and thrashing
as it has no eyelids. The confamilial common scaly foot
(Pygopus lepidopodus), which feeds on arthropods,
cannot retract its eyes nearly as dramatically (M.
Wall, pers. observ.), so this ability is likely derived in
L. burtonis.
Other predators that commonly take large and/or
dangerous prey animals also have evolved means of
protecting their vulnerable eyes. For example, many
sharks slide a thick, protective nictitating membrane
over their eyes during feeding episodes (Gilbert, 1963).
Narrowmouth toads (Gastrophryne spp.), which prey
extensively upon ants, possess a fold of skin across the
back of the head which can be moved forward to shield
their eyes from bites and stings (Conant & Collins,
1991). Similarly, scolecophidians (blindsnakes and
threadsnakes) subsist primarily on the larvae and
pupae of ants, requiring them to infiltrate ant nests
(Punzo, 1974; Webb & Shine, 1993a; Webb et al., 2000,
2001). The reduced eyes of these small, basal snakes
are covered by scales (Cogger, 2000), preventing ants
from exploiting a potential chink in their armour of
smooth, glossy scutellation.
In advanced snakes, constriction, venom, and the
strategy of striking and releasing prey also all serve to
protect the eyes; many snakes utilizing these mea-
725
sures are visually orientated ambush foragers that
may take very large prey (e.g. vipers and boids;
Greene, 1997). However, selective pressure to protect
the eyes may be stronger on L. burtonis than it is on
vipers, boas and pythons, for the thermal imaging
capabilities of these snakes allow them to compensate
to a large degree for compromised vision (Kardong,
1992; Grace & Woodward, 2001; Grace et al., 2001).
Eye retraction, precision striking, the subdual of very
large prey, and morphological characters such as a
long snout and hinged, pointed, and recurved teeth all
contribute to keeping the eyes of L. burtonis from
harm.
The convergence between L. burtonis and snakes
is remarkable. In an ecological sense, L. burtonis is
essentially an ambush-foraging snake; it is functionally limbless and feeds at infrequent intervals on relatively large prey (Patchell & Shine, 1986a, b, c; Huey
et al., 2001). The present study illustrates one more
aspect of this convergence: like snakes, L. burtonis
has evolved several measures minimizing the risk of
injury while tackling large prey animals. Furthermore, the fact that both snakes and L. burtonis exhibit
such parallel strategies argues strongly that prey
defensive capabilities are a significant force in predator evolution. Many of the weapons that predators
employ to dispatch prey, such as the extremely toxic
venom of many snakes, should thus be regarded as
both offensive and defensive adaptations.
ACKNOWLEDGEMENTS
Funding was provided to M.W. by a National Science
Foundation (USA) Graduate Research Fellowship and
to R.S. by the Australian Research Council.
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