JOURNAL OF EXPERIMENTAL ZOOLOGY 309A:447–459 (2008)
A Journal of Integrative Biology
Horned Lizards (Phrynosoma) Incapacitate Dangerous Ant
Prey With Mucus
WADE C. SHERBROOKE1 AND KURT SCHWENK2
Southwestern Research Station, American Museum of Natural History, Portal,
Arizona
2
Department of Ecology and Evolutionary Biology, University of Connecticut,
Storrs, Connecticut
1
ABSTRACT
Horned lizards (Iguanidae, Phrynosomatinae, Phrynosoma) are morphologically
specialized reptiles characterized by squat, tank-like bodies, short limbs, blunt snouts, spines and
cranial horns, among other traits. They are unusual among lizards in the degree to which they
specialize on a diet of ants, but exceptional in the number of pugnacious, highly venomous, stinging
ants they consume, especially harvester ants (genus Pogonomyrmex). Like other iguanian lizards, they
capture insect prey on the tongue, but unlike other lizards, they neither bite nor chew dangerous prey
before swallowing. Instead, they employ a unique kinematic pattern in which prey capture, transport
and swallowing are combined into a single feeding stage, apparently leaving the mouth, pharynx,
esophagus and stomach vulnerable to bites and stings. Nevertheless, horned lizards consume dozens of
harvester ants without harm. We show that their derived feeding kinematics are associated with
unique, mucus-secreting pharyngeal papillae that apparently serve to immobilize and incapacitate
dangerous ants as they are swallowed by compacting them and binding them in mucus strands.
Radially branched esophageal folds provide additional mucus-secreting surfaces the ants pass through
as they are swallowed. Ants extracted from fresh-killed horned lizard stomachs are curled ventrally
into balls and bound in mucus. We conclude that the pharyngeal papillae, in association with a unique
form of hyolingual prey transport and swallowing, are horned lizard adaptations related to a diet of
dangerous prey. Harvester ant defensive weapons, along with horned lizard adaptations against such
weapons, suggest a long-term, predator–prey, co-evolutionary arms race between Phrynosoma and
r 2008 Wiley-Liss, Inc.
Pogonomyrmex. J. Exp. Zool. 309A:447–459, 2008.
How to cite this article: Sherbrooke WC, Schwenk K. 2008. Horned lizards (Phrynosoma)
incapacitate dangerous ant prey with mucus. J. Exp. Zool. 309A:447–459.
Horned lizards, genus Phrynosoma (Squamata,
Iguanidae), are small, bizarrely derived reptiles
(Fig. 1) ranging across the American west from
southern Mexico to southern Canada. They are
particularly abundant in the deserts of the southwestern United States and northern Mexico
(Sherbrooke, 2003). They belong to a diverse clade
of iguanid lizards known as ‘‘phrynosomatines’’
(Schulte et al., 2003; traditionally called ‘‘sceloporines,’’ Etheridge and de Queiroz, ’88), but
often accorded familial status as the Phrynosomatidae (Frost and Etheridge, ’89). This clade
includes several generalized, basal genera as well
as a more derived, monophyletic group known as
the ‘‘sand lizards’’ (Uma, Callisaurus, Cophosaurus and Holbrookia). Phrynosoma is regarded
as the sister group of the sand lizard clade (Wiens,
r 2008 WILEY-LISS, INC.
’93; Reeder and Wiens, ’96; Wilgenbusch and de
Queiroz, 2000; Leaché and McGuire, 2006; Schulte
and de Queiroz, 2008) (Fig. 2).
Most lizards eat a variety of prey types,
especially small invertebrates. Dietary specialization, in the sense of stenophagy, is relatively
uncommon among lizards and phenotypic specia-
Grant sponsor: National Science Foundation; Grant number: NSF
IBN-9601173; Grant sponsor: University of Connecticut Research
Foundation.
Both authors contributed equally to this paper.
Correspondence to: Kurt Schwenk, Department of Ecology and
Evolutionary Biology, University of Connecticut, Storrs, CT 062693043. E-mail: kurt.schwenk@uconn.edu
Received 9 August 2007; Revised 6 May 2008; Accepted 13 May
2008
Published online 20 June 2008 in Wiley InterScience (www.
interscience.wiley.com). DOI: 10.1002/jez.472
448
W.C. SHERBROOKE AND K. SCHWENK
lization of the feeding apparatus reflecting a
specialized diet is even less common (Greene,
’82; Schwenk, 2000b; Pianka and Vitt, 2003;
Schwenk and Rubega, 2005). Thus, horned lizards
Fig. 1. A Texas horned lizard, Phrynosoma cornutum,
showing the tank-like body, short limbs, cranial horns and
other morphological features typical of the genus and often
erroneously attributed to myrmecophagy (see text).
A
are unusual in the degree to which most species
specialize on a diet of ants. It is, therefore, not
surprising that their highly derived and unusual
morphology is widely believed to reflect their
myrmecophagous habits. In this study we examine
the functional morphology of ant consumption in
horned lizards and consider the question of dietspecific adaptation.
Although most species of Phrynosoma eat other
prey types, sometimes in significant quantities,
ants are nearly always the most important type
numerically and many species consume ants
almost exclusively (Norris, ’49; Pianka, ’66;
Pianka and Parker, ’75; Whitford and Bryant,
’79; Rissing, ’81; Turner and Medica, ’82; Suarez
et al., 2000; Lahti and Beck, 2008). In a classic
study of Phrynosoma ecology, Pianka and Parker
(’75:156) concluded that horned lizards encompass
a ‘‘unique constellation of anatomical, behavioral,
physiological and ecological adaptations that facilitate efficient exploitation of ants as a food source
Sceloporus
Sator
Urosaurus
Petrosaurus
Uta
Phrynosoma
Uma
Callisaurus
Cophosaurus
Holbrookia
B
Holbrookia
Cophosaurus
Callisaurus
Uma
Phrynosoma
Sceloporus
Urosaurus
Uta
Fig. 2. Phylogenetic relationships among phrynosomatine lizards. Note that in both hypotheses, Phrynosoma is the sister
taxon to a monophyletic group of genera known as the ‘‘sand lizards.’’ Based on mitochondrial and nuclear DNA sequences,
Leaché and McGuire (2006) found a similar sister relationship between Phrynosoma and the sand lizards with the exception
that the positions of Uma and Callisaurus were reversed. (A) Relationships according to Wiens (’93) and Reeder and Wiens (’96)
based on morphology and mitochondrial DNA sequence data. (B) Relationships according to Wilgenbusch and de Queiroz (2000)
based on mitochondrial DNA sequence data.
J. Exp. Zool.
HORNED LIZARDS INCAPACITATE DANGEROUS PREY WITH MUCUS
and set [them] apart from most other species of
lizards.’’ These features include a squat, tank-like
body that is dorsoventrally compressed, scaly
spines, short limbs, a short tail, a head with
blunted snout and posteriorly directed cranial
horns, large stomach volume, relaxed thermoregulation and specialized foraging techniques,
among others (Fig. 1). Many of these attributes
may be a consequence of the poor nutritional
quality of ants (Redford and Dorea, ’84), which
requires myrmecophages to consume them in
large numbers, often at exposed colony sites.
According to Pianka and Parker (’75), horned
lizards adapted to the challenge of feeding on
small, nutritionally poor prey by increasing stomach volume relative to body size so that they
could consume the ants in large numbers. This
putatively led to a reduction in locomotor speeds
that, in conjunction with exposure during foraging
in open habitats, led, in turn, to adaptations for
increasing levels of predator defense, including
cryptic coloration, freezing as a response to alarm,
horns, spines, blood-squirting of defensive chemicals, etc. (Pianka and Parker, ’75; Sherbrooke and
Middendorf, 2001, 2004; Sherbrooke, 2003; Young
et al., 2004). As such, horned lizards feed on many
small prey items (ants) that are unevenly distributed (i.e., clumped) within open habitats that
afford little cover or protection from visually
hunting predators. Although the derived horned
lizard phenotype is often assumed to reflect
dietary specialization (e.g., Hotton, ’55; Whitford
and Bryant, ’79; Schmidt and Schmidt, ’89;
MacMahon et al., 2000), most of the lizards’
unusual morphology and behavior is actually
attributable to selection stemming from predation
pressure and resource competition only indirectly
related to feeding on ants. In other words, most
aspects of the derived horned lizard phenotype
reflect the circumstances under which the lizards
feed rather than the food they feed on. No
adaptations of the trophic apparatus related
directly to a diet of ants have been demonstrated
for Phrynosoma thus far.
In fact, many lizards eat ants without any
apparent phenotypic specialization (reviewed by
Schwenk, 2000b; Pianka and Vitt, 2003; Vitt et al.,
2003). However, horned lizards are exceptional—
probably unique—in the number of dangerous,
highly venomous ants included in their diets,
particularly harvester ants of the genus Pogonomyrmex (Formicidae) (Pianka and Parker, ’75;
Whitford and Bryant, ’79; Rissing, ’81; Turner and
Medica, ’82; Schmidt and Schmidt, ’89; Schmidt
449
et al., ’89; Suarez et al., 2000). Indeed, several
horned lizard species eat almost nothing else. In
contrast, most lizards select more nutritious prey
and avoid dangerous prey as much as possible
(Vogel and von Brockhusen-Holzer, ’84; Hasegawa
and Taniguchi, ’93, ’96; López and Martı́n, ’94;
Vitt et al., 2003). A closely related sand lizard,
Uma inornata, for example, only resorts to feeding
on Pogonomyrmex ants in drought years when
other insects are unavailable. The lizards fail to
thrive on this diet and lose weight (C. W. Barrows,
personal communication).
Harvester ants have powerful mandibles for
cropping seeds (Hermann and Blum, ’81; Schmidt
and Schmidt, ’89) and these are also used
defensively against predators, including horned
lizards (Schmidt and Blum, ’78; Hermann and
Blum, ’81; Schmidt and Schmidt, ’89; Sherbrooke,
personal observation). In addition, Pogonomyrmex
ants have an autotomizing sting (i.e., one that
breaks off in the victim) that injects a potent
venom. Stinging is used solely as a defensive
weapon (Cole, ’68; Hermann and Blum, ’81;
Schmidt and Schmidt, ’89). One species
(P. maricopa) produces the most toxic venom
known for any arthropod (according to LD50
studies with mice [Schmidt and Schmidt, ’89]).
Sting autotomy is thought to have evolved in ants
specifically as a defense against vertebrate predators (Hermann, ’71; Schmidt and Blum, ’78;
Kugler, ’79; Hermann and Blum, ’81; Schmidt and
Schmidt, ’89). In humans Pogonomyrmex stings
cause excruciating pain (Cole, ’68; Schmidt and
Schmidt, ’89). However, horned lizards are less
sensitive to Pogonomyrmex venom than related
lizards because of a blood plasma factor that
detoxifies the venom to some extent (Schmidt and
Schmidt, ’89; Schmidt et al., ’89). Nonetheless,
they are not immune—the venom is fatal if a
lizard is stung too many times (Edwards, 1896;
Schmidt et al., ’89).
While foraging, horned lizards must balance the
need to maximize the number of ants consumed
with the need to avoid mobbing (and potentially
fatal stinging) by an aroused colony, as well as the
need to minimize movements that might attract
predators. They have evolved an unusual foraging
strategy in which they move through the environment seeking columns of foraging ants, whereupon they remain still (Whitford and Bryant, ’79;
Rissing, ’81; Shaffer and Whitford, ’81; Munger,
’84), capturing ants with exceptional speed by
using precisely targeted tongue protrusion and
rapid prey handling (see below; Schwenk, 2000b,
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450
W.C. SHERBROOKE AND K. SCHWENK
and unpublished data; Ott et al., 2004, and
unpublished data; Meyers and Herrel, 2005). Before
the ant colony can respond defensively, the lizards
cease predation and move on in search of another
column (Whitford and Bryant, ’79; Rissing, ’81).
Like other members of the iguanian clade
(Iguanidae, Agamidae and Chamaeleonidae),
horned lizards capture small prey with the tongue
(Schwenk and Throckmorton, ’89; Schwenk,
2000b; Meyers and Herrel, 2005). They are able
to modulate tongue trajectory and distance as they
target fast-moving ant prey using rapid head
movements in response to visual feedback (Ott
et al., 2004, and unpublished data). Our initial
observations suggested that, unlike other insectivorous lizards, horned lizards neither bite nor
chew captured ants before swallowing (Schwenk,
2000b; Schwenk and Sherbrooke, 2003; Sherbrooke, 2003; Ott et al., unpublished data). Therefore, during prey capture, intraoral transport and
swallowing, they potentially expose the vulnerable
soft tissues of the mouth and pharynx to bites and
stings. In contrast, other lizards that only occasionally eat stinging hymenopterans or other
dangerous prey adopt an unusual capture and
processing behavior involving rapid biting and
chewing to kill the prey before it can sting (Vitt
and Cooper, ’88; O’Connell and Formanowicz, ’98;
Lappin and German, 2005; C. W. Barrows,
personal communication). However, killing each
prey item by biting or chewing incurs a significant
cost in handling time, and this may make such a
strategy unfeasible for horned lizards (see below).
In this study we address the problem of how
horned lizards are able to consume large numbers
of pugnacious, biting, stinging, highly venomous
ants without being injured or killed in the process.
MATERIALS AND METHODS
We examined feeding behavior in Texas horned
lizards (P. cornutum, n 5 4) using high-speed (250
frames per sec) 16 mm cine film and frame-byframe motion analysis. During filming, lizards
were fed small, juvenile crickets comparable in
size to Pogonomyrmex ants. We also examined the
stomach contents of ten fresh, road-killed specimens of P. cornutum from southwestern New
Mexico with particular attention to prey condition.
Finally, we used standard paraffin histology to
examine the microscopic anatomy of the mouth
and pharynx (n 5 4). Specimens were decalcified in
formic acid A solution (Presnell and Schreibman,
’97), sectioned at 8–10 mm and stained with either
J. Exp. Zool.
Ehrlich hematoxylin and eosin or Weigert iron
hematoxylin and picro-ponceau (protocols slightly
modified from Presnell and Schreibman, ’97 and
available on request from K. S.). We compared our
results to similar sections made of other Phrynosoma species (P. asio, P. coronatum, P. hernandesi,
P. douglasii, P. modestum, P. mcallii, P. orbiculare, P. platyrhinos and P. solare), as well as sister
and outgroup taxa including the sand lizards (C.
draconoides, U. scoparia, C. texanus, H. maculata), other phrynosomatines (Sceloporus spp., Urosaurus graciosus, Uta stansburiana), other
iguanids, agamids and more distant, noniguanian,
taxa (including representatives of all lizard families). Included in our outgroup samples were
other ant-eating lizards such as Anolis bonairensis, Liolaemus monticola (Iguanidae) and the
agamids Draco volans and Moloch horridus. We
also examined the morphology of the esophagus in
P. cornutum, P. modestum, P. platyrhinos, P.
mcallii, P. hernandesi, P. coronatum and P. solare,
and compared our results with data in the
literature for other squamates.
RESULTS
Feeding kinematics
Horned lizards capture prey using a mostly
typical iguanian lizard pattern of lingual prehension (Schwenk and Throckmorton, ’89; Schwenk,
2000b; Meyers and Herrel, 2005). They differ
slightly from other iguanid species in protruding
the tongue relatively farther (tongue protrusion
distance/jaw length 5 0.50 as compared with
0.17–0.31; some agamids have comparable protrusion distances, however; Schwenk and Throckmorton, ’89) and in having a derived tongue and
hyobranchial morphology (Schwenk, ’94, and in
preparation). However, they show dramatic departures from other iguanian taxa in two ways.
First, the films confirmed that the teeth are not
used at all to chew or crush small prey after
capture (Fig. 3A–C) (noted also in P. platyrhinos;
Schwenk, unpublished data; Meyers and Herrel,
2005). In contrast, the usual iguanian pattern is to
place the prey item between upper and lower tooth
rows for killing and chewing immediately upon
capture (Fig. 3D–F) (Schwenk and Throckmorton,
’89; Schwenk, 2000b). Second, horned lizards
exhibit a unique hyolingual behavior after lingual
retraction of prey into the mouth (Fig. 3A–C).
Retraction is extremely fast (approx. 30 msec) and
in a single motion the prey item is pulled past the
teeth postero-ventrally, deep into the pharynx and
HORNED LIZARDS INCAPACITATE DANGEROUS PREY WITH MUCUS
directly to the esophagus. This is evident externally as a pronounced bulge in the throat caused
by movement of the tongue and hyobranchial
apparatus. Swallowing is coincident with this
behavior so that when the tongue is once again
protracted, the prey item has disappeared from
the oral cavity and pharynx. This behavior contrasts sharply with other iguanians in which such
extreme bulging is evident neither during lingual
prey capture, nor during processing, transport and
swallowing cycles (Fig. 3D–F). Furthermore, in
other lizards intraoral transport and swallowing
are accomplished during separate, kinematically
distinct hyolingual cycles that are independent of
the ingestion (prehension/capture) stage. As such,
451
the merging of ingestion, transport and swallowing into a single feeding (ingestion) stage in
Phrynosoma is exceptional, if not unique (see
Schwenk, 2000a,b and Schwenk and Rubega,
2005, for reviews of feeding stages in lizards and
other vertebrates).
Horned lizards often exhibit several low-amplitude gape and hyolingual cycles after the initial
ingestion cycle (see Schwenk, 2000b, Fig. 8.22), as
if clearing the mouth and pharynx of extraneous
material. We did not offer our lizards prey in rapid
sequence, as would be typical in the field, and it is
possible that these extraneous cycles would be
eliminated under such circumstances. An entire
ingestion cycle, from prehension to swallowing,
Fig. 3. The kinematics of lingual prehension in a horned lizard (P. cornutum) and a generalized iguanid lizard (desert
iguana, Dipsosaurus dorsalis). (A–C) Three individual frames from a feeding sequence in P. cornutum showing retraction of the
prey item into the mouth on the tongue’s surface. Note the extreme ventral bulge of the gular region as the tongue and
hyobranchial apparatus are retracted postero-ventrally. During this rapid movement (approx. 30 msec total), the prey item is
forced through the pharyngeal papillae where it is balled, bound in mucus and pushed into the esophagus—an action that
combines in one feeding stage/jaw cycle the typically disparate stages of ingestion, processing, transport and swallowing. (D–F)
Typical iguanian lizards, such as this desert iguana, capture prey on the tongue and then crush it between the teeth (this is true
even for smaller prey then shown). Note that the transit of the hyolingual apparatus is modest and little gular bulging is evident.
Separate chewing, transport and swallowing cycles usually follow ingestion and are not accompanied by the kind of extreme
gular bulging evident in horned lizards (A–C). Pharyngeal papillae are lacking. Compare also Figs. 4 and 5 in Meyers and Herrel
(2005) showing ingestion in Uma notata and P. platyrhinos.
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W.C. SHERBROOKE AND K. SCHWENK
takes approximately 60 msec, although protrusion
time and distance can be modulated so that longer
times are often observed (Ott et al., 2004).
Although for our film trials we fed the horned
lizards baby crickets, our personal observations, as
well as high-speed video recordings (Ott et al.,
unpublished data), of Phrynosoma feeding on
Pogonomyrmex ants confirm that they use identical feeding kinematics. Horned lizards seem to
employ a stereotyped feeding behavior when
feeding on a variety of prey types (W. C. S. and
K. S., personal observation). As such, there is no
reason to believe that our film observations are an
artifact of feeding the lizards a non-ant prey type.
Condition of ants in stomach
Stomachs of fresh, road-killed specimens were
packed with dozens of Pogonomyrmex and other
ants. Most ants were intact, although the heads of
some had broken off. The ants were almost
certainly alive when initially swallowed (e.g.,
Sherbrooke, 2002; see below). Isolated, individual
ants were encased within mucus, usually curled
ventrally into a compact ball, with limbs, antennae, mandibles, body segments and stingers bound
together by strands of mucus (Fig. 4). This
observation suggests circumstantially that during
passage through the esophagus, each ant is
immobilized so that stinging and/or biting would
be impossible.
Histology of the pharynx and esophagus
In all Phrynosoma species examined, gross
examination and histological sections revealed
that the ventral surface of the pharynx is covered
by a deep pile of long papillae, densely covered
with columnar mucocytes (Figs. 5, 6). Thiomine
staining confirmed that the mucocytes are secretory cells rich in mucopolysaccharides. The long,
mucous papillae typically extend from the posterior portions of the tongue, over the larynx and the
trachea, and throughout the ventral portion of the
pharynx. The pharyngeal papillae are oriented
posteriorly, slightly overlapping those behind
(Figs. 5A, 6B, D, E). Note that the lingual
morphology of Phyrnosoma is highly derived
relative to other iguanians (Schwenk, ’94; in
preparation). One derived characteristic is the
separation of the genioglossus lateralis muscles
from the flanks of the tongue body so that they
insert much farther posteriorly compared with
other species, forming prominent ridges alongside
the tongue proper (Fig. 5; compare to Sceloporus).
The papillae that cover these muscles and the back
end of the tongue are unusually long and robust;
they are unlike the lingual papillae typically found
Fig. 4. Photomicrographs of ants extracted from the stomachs of fresh, road-killed specimens of P. cornutum in New
Mexico. (A) A small group of ants balled and bound in mucus; (B–D) individual harvester ants (Pogonomyrmex sp.) tightly
bound in mucus. Note that each ant is curled ventrally into a ball, bound by strands of mucus and presumably incapacitated,
though it may remain alive in the gut for some time. The stomach may be further protected by mucus that forms a discrete sac
lining the stomach (Lahti et al., in preparation).
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HORNED LIZARDS INCAPACITATE DANGEROUS PREY WITH MUCUS
453
Fig. 5. Photomicrographs illustrating the gross form of the lower jaw, tongue, larynx and floor of the pharynx in two
phrynosomatine lizards. (A) A horned lizard, P. douglasii, showing the unusual tongue morphology and the thick carpet of
robust, mucous papillae covering the posterior limbs of the tongue, the larynx (dark central hole is the glottis) and the floor of
the pharynx posterior to the tongue. The papilla-covered bands of tissue curving on either side of the tongue are the
genioglossus lateralis muscles that in other lizards form the lateral walls of the tongue, but in horned lizards are discrete
(Schwenk, ’94 and in preparation). The tongue, itself, is covered with much finer papillae used during prey prehension on the
tongue’s anterior surface (see Schwenk, 2000b). (B) Tongue and pharyngeal form in a generalized, basal phrynosomatine,
Sceloporus sp. Note the lack of papillae on the larynx and the floor of the pharynx. The pharynx is covered, instead, with thin
striations and a typical mucous epithelium (see Fig. 6G). The form of the pharynx in this species is typical of most lizards.
on this part of the tongue (e.g., Schwenk ’88) and
histologically appear to be an anterior extension of
the ‘‘pharyngeal’’ papillae described here.
Pharyngeal papillae end abruptly at the beginning of the esophagus where they are replaced by
longitudinal folds running the length of the
esophagus to the stomach. The folds comprise
major and minor parts; each major fold represents
a set of several radially branching minor folds or
pleats, visible as longitudinal striations on the
surface of each major fold (Fig. 7). Each pleat is
covered with a dense layer of goblet cells that
release their mucus into the longitudinal grooves
between pleats (Fig. 7C). Note that in Figures 7A
and B the esophagus has been slit longitudinally
and flattened to visualize the luminal surface. In
life, however, the folds project well into the
esophageal lumen, virtually occluding it (Fig.
7C). Thus, engulfment of ants in mucus-secreting
tissues would be undiminished as they travel
throughout the pharynx and esophagus to the
stomach.
In all sister and outgroup species examined,
pharyngeal papillae are entirely absent (e.g.,
Fig. 6H, I, J), or are only weakly developed
(e.g., Fig. 6F, G). Within the phrynosomatines,
basal taxa (Sceloporus, Urosaurus and Uta), as
well as two sand lizard taxa (Callisaurus and
Uma) lack pharyngeal papillae completely,
whereas Cophosaurus and Holbrookia exhibit very
weakly developed papillae (which become even less
developed posterior to the sections illustrated in
Fig. 6). Pharyngeal papillae are absent in all more
distant outgroup taxa, as well. As an outgroup
control, we included in our study several iguanian
taxa that are putative ant specialists (A. bonairensis, L. monticola, D. volans, M. horridus; see
Schwenk, 2000b, Table 8.6, for references). All of
these taxa completely lack pharyngeal papillae
(e.g., Fig. 6J). These results strongly suggest that
the well-developed, mucus-secreting pharyngeal
papillae present in all Phrynosoma species examined are uniquely derived within the genus.
Evolutionary inferences about esophageal morphology in Phrynosoma are more tentative because we did not undertake a systematic study of
the esophagus for this study and published data
are inadequate for comparative purposes. Longitudinal folds and striations are typical of the
esophagus in most squamate reptiles, as are
mucus-secreting goblet cells (Luppa, ’76; Parsons
and Cameron, ’76; Imai and Shibata, ’92; Loumbourdis, 2003). Indeed, longitudinal folds are
typical of most vertebrates owing to the need for
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W.C. SHERBROOKE AND K. SCHWENK
HORNED LIZARDS INCAPACITATE DANGEROUS PREY WITH MUCUS
455
Fig. 7. Surface morphology and histology of the esophagus in Phrynosoma. (A) Gross morphology of the luminal surface in
P. cornutum. Anterior is at the top. Note the major folds and their longitudinal striations indicating the minor folds, or pleats.
(B) A digital enlargement of (A) delimiting the major folds and pleats with long and short lines, respectively. (C) Transverse
section of the esophagus in P. solare (H & E). Note the extreme development of the major folds (long line) and the radial
branching of pleats (short line) within each major fold. In situ the folds virtually occlude the lumen () Each pleat is covered by a
dense mucous epithelium such that the mucus drains into the clefts between pleats. No scale bars available.
the esophagus to expand during swallowing of
food. However, in only a few squamate species
examined (e.g., Agama [Stellio] stellio and Natrix
sp.) is there evidence of three-dimensional relief
significant enough to cause luminal occlusion
approaching what we observe in Phyryosoma
(Luppa, ’76; Loumbourdis, 2003). We can find no
evidence that any other taxa exhibit the radial
branching of the major folds into pleats (a
morphology that greatly enhances the surface
area of the mucus-secreting epithelium). Thus, it
is possible that the esophagus in Phrynosoma is
derived both quantitatively and qualitatively as
compared with other squamates (in the relative
development of the longitudinal folds and in the
subdivision of the folds into pleats that increase
mucosal surface area, respectively). Any such
conclusion must be verified by additional, comparative data, however, particularly for other
phrynosomatine species. Regardless, it is clear
Fig. 6. Histology of the pharynx in phrynosomatine lizards. In all cases the scale bar 5 1 mm. (A) P. cornutum, transverse
section, showing pharyngeal papillae covering the larynx. Red-staining tissue is the collagenous, connective tissue core of the
papillae; the yellowish-tan tissue is the mucous epithelium covering the sides of the papillae. In the transverse plane the papillae
are complex and often form anastomoses with mucous crypts. Weigert hematoxylin and picro-ponceau stain (H & PP). (B) P.
cornutum, mid-sagittal section, of the larynx. Anterior is to the left. The space at the bottom of the picture is the lumen of the
trachea; note the purple-staining laryngeal cartilages below. Long pharyngeal papillae extend dorsally and slightly posteriorly.
Mucocytes covering the papillae are stained pale pinkish-lavender. The epithelium at the papillary apices is nonmucous and
stains more darkly. This photograph was taken without reference to a scale, so no scale bar is present, but the scale is similar to
the other photos. Ehrlich hematoxylin and eosin stain (H & E). (C–D) P. coronatum, transverse and mid-sagittal sections,
respectively (H & E). (E) P.orbiculare, mid-sagittal section, showing larynx and the opening of the glottis at the back of the
tongue to the left (H & PP). (F) Uma scoparia, a sand lizard, transverse section through the larynx showing weakly developed
pharyngeal papillae mostly lacking mucus cells (H & E). (G) Holbrookia maculata, another sand lizard, transverse section
through the larynx showing weakly developed pharyngeal papillae with a mucous epithelium. In sand lizards, the minimal
pharyngeal papillae do not extend very far posteriorly (H & PP). (H) Sceloporus occidentalis, a basal phrynosomatine, parasagittal section through larynx with posterior end of the tongue at left. The yellow-staining tissue is primarily lingual and
intrinsic laryngeal muscle. Note smooth surface of the pharyngeal epithelium dorsally. Only the occasional goblet cell is evident.
This type of featureless, nonpapillose epithelium is characteristic of nearly all lizards examined (H & PP). (I) Uta stansburiana,
another basal phrynosomatine, mid-sagittal section through the larynx (H & E). (J) Anolis bonairensis, an ant-eating iguanid
unrelated to horned lizards and other phrynosomatines, showing a complete absence of pharyngeal papillae. Transverse section
(H & PP).
J. Exp. Zool.
456
W.C. SHERBROOKE AND K. SCHWENK
that the structure of the horned lizard esophagus
would further promote mucus binding of ants as
they move to the stomach.
DISCUSSION
Our data provide strong circumstantial evidence
that horned lizards are able to consume dangerous
ants by immobilizing them with mucus within the
pharynx immediately after capture. Mucus binding presumably occurs when the ants are pushed
deep into the papillae by the tongue, simultaneously expressing mucus from the papillae,
compacting the ant and incapacitating its weapons
(mandibles and stinger). This phase of the process
is evident externally as pronounced gular bulging,
reflecting extreme postero-ventral retraction of
the hyolingual apparatus as the insect is transported through the pharyngeal papillae and into
the esophagus. This scenario is also supported by
high-speed video images of feeding P. cornutum
that reveal thick strands of mucus running across
the pharynx when the mouth is opened (Ott et al.,
unpublished data). Most iguanian lizards swallow
by pushing food into the esophagus with posterior
lobes of the tongue in a cyclical behavior known as
‘‘pharyngeal packing’’ (Smith, ’84; Schwenk,
2000b). Horned lizards, however, are exceptionally
short-necked and the pharynx is correspondingly
abbreviated so that the ant is pushed directly into
the esophagus after traversing the pharyngeal
papillae. Horned lizards, therefore, combine the
three stages of ingestion, transport and swallowing typically seen in lizards into a single feeding
stage. Prey processing with the jaws and teeth,
also evident in most lizards, is eliminated and
replaced with a unique form of pharyngeal prey
processing.
The precise manner in which ants are transported through the pharyngeal papillae to the
esophagus and bound with mucus remains unclear. Preliminary data suggest that horned
lizards deform the posterior end of the tongue in
an unusual way during this transport process and
that the tongue exhibits several derived attributes
that might be related to this behavior (Schwenk,
unpublished data).
Crushing ants with the teeth might be a simpler
way to render them harmless, but this may not be
feasible in horned lizards because the time
required to position prey between the teeth for
chewing could allow an ant to bite or sting
vulnerable oral tissues. By immobilizing ants
almost immediately after prey capture, horned
J. Exp. Zool.
lizards disable the ant’s weapons before they can
be used defensively. Furthermore, by substituting
single-cycle pharyngeal processing for multiple
cycles of chewing, transport and swallowing,
horned lizards are able to reduce dramatically
the handling time of individual prey items.
Handling time is especially important for horned
lizards because they feed rapidly on multiple prey
items during a single feeding bout as they pick-off
individual ants from foraging columns. They
consume as many ants as possible in a short time
so that they can move on to another colony before
being detected and mobbed by aggressive ant
workers, or attacked by predators. Indeed, Meyers
and Herrel (2005) showed that the specialized ant
eaters, P. platyrhinos and M. horridus (Agamidae), differed from other lizards in the rapidity of
their feeding events owing to the elimination of an
oral processing stage.
Small movements of ants in the pharynx and
esophagus of horned lizards have been visualized
by X-ray videography, demonstrating that ants
remain alive as they are swallowed (J. Meyers,
personal communication). Presumably, insects not
crushed by chewing remain alive in a lizard’s gut
for some time before chemical digestion. By
incapacitating the ants’ weapons at the time of
capture, horned lizards not only avoid bites and
stings within the mouth and throat, but also in the
stomach. The reality of this danger is indicated by
the deaths of several round-tail horned lizards
(P. modestum) kept in outdoor enclosures (Sherbrooke, 2002). Postmortem examination revealed
that the lizards had died after consuming large
beetles that had bored through their stomachs.
P. modestum’s mucus-binding defense was probably ineffective because of the beetles’ size, form
and strength or possibly because this small horned
lizard species has secondarily reduced its dietary
dependence on Pogonomyrmex ants (Whitford and
Bryant, ’79; Shaffer and Whitford, ’81; Munger,
’84; Schwenk and Sherbrooke, in preparation).
To our knowledge the mucus prey-binding
system we describe is unique among vertebrates.
Mammalian myrmecophages, especially edentates
and pangolins, have exceptionally large salivary
glands and sticky mucus that coats the tongue for
prey adhesion (e.g., Doran and Allbrook, ’73;
Reiss, 2000), and this might passively incapacitate
some dangerous ants. However, mammals in
general avoid exposure to dangerous ant species
(Swart et al., ’99) and feed preferentially on
harmless and more nutritious termites. Mammalian myrmecophages do share some interesting
HORNED LIZARDS INCAPACITATE DANGEROUS PREY WITH MUCUS
attributes of the feeding apparatus with horned
lizards, notably lingual prehension of prey, copious salivary mucus, reduced bite forces and lack
of oral processing (Reiss, 2000; Meyers et al.,
2006).
Some marine turtles have heavily keratinized
pharyngeal and esophageal papillae, but these
only protect the pharyngeal surfaces against
abrasion and stings (respectively) from the
silicaceous sponges and medusae they consume,
as well as directing the gelatinous prey toward
the esophagus (e.g., Schumacher, ’73; Parsons
and Cameron, ’76; Meylan, ’88; Winokur, ’88);
they do not disarm the prey item, itself. Some
freshwater, pelomedusid (side-necked) turtles
have similar, but unkeratinized papillae in the
esophagus (Parsons and Cameron, ’76; Vogt et al.,
’98), but these are believed to serve as filters to
retain small food items in the gut during water
expulsion after feeding (Belkin and Gans, ’68;
Vogt et al., ’98).
We have shown that horned lizards possess
several uniquely derived traits—a single, combined
ingestion/transport/swallowing stage, elimination
of chewing cycles, pronounced postero-ventral
hyolingual retraction, and mucus-secreting pharyngeal papillae—that we infer to be a character
complex functionally related to incapacitating the
weapons of the dangerous ant prey they consume
in large numbers. It is reasonable to conclude that
these traits represent adaptations to their specialized diet. Nonetheless, it is important to recognize that such adaptations are not a response to
myrmecophagy, per se, but rather reflect the need
to cope with highly defended, dangerous prey.
Thus, many lizards are able to consume large
quantities of ants without apparent phenotypic
specialization (Schwenk, 2000b). Other than their
low nutritional value, most ants do not seem to
pose a particular challenge to the generalized
lizard feeding system (Schwenk, 2000b; Vitt et al.,
2003). This finding highlights the fact that it is a
food item’s mechanical attributes, rather than its
taxonomic affiliation, that mediates the evolutionary link between dietary and phenotypic specialization (see discussion in Schwenk, 2000b). The
presence of effective antipredator, defensive weapons in harvester ants and unique adaptations
(behavioral, morphological and physiological) to
cope with these weapons in horned lizards
suggests the possibility of a long-standing predator–prey, co-evolutionary arms race in this
system, a hypothesis we are presently exploring
(Schwenk and Sherbrooke, in preparation).
457
ACKNOWLEDGMENTS
We are grateful to Tobias Landberg, Jonathan
Richmond, Margaret Rubega, Chuck Smith, Kentwood Wells and an anonymous reviewer for
commenting on and improving earlier versions of
the manuscript. Cameron Barrows generously
shared his observations and unpublished manuscript on fringe-toed lizards. Philip Fernandez
provided a thiamine stained section of a
P. cornutum pharynx for us to examine. Jay
Meyers permitted us to cite his unpublished,
X-ray vidographic observations and Matthias Ott
allowed us to cite unpublished data on P. cornutum capture of Pogonomyrmex ants. Work was
supported by grants from the National Science
Foundation (NSF IBN-9601173) and the University of Connecticut Research Foundation to K. S.
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