Antipredator Nest Guarding by Female Horned Lizards (Phrynosoma): Iguanian

Parental Care
Author(s): Wade C. Sherbrooke
Source: Herpetologica, 73(4):331-337.
Published By: The Herpetologists' League
URL: http://www.bioone.org/doi/full/10.1655/Herpetologica-D-17-00028.1

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Herpetologica, 73(4), 2017, 331–337
Ó 2017 by The Herpetologists’ League, Inc.

Antipredator Nest Guarding by Female Horned Lizards (Phrynosoma):

Iguanian Parental Care
WADE C. SHERBROOKE1
Southwestern Research Station, American Museum of Natural History, Portal, AZ 85632, USA

ABSTRACT: This is the first report of antipredator nest defense by iguanian lizards. Female Texas Horned Lizards (Phrynosoma cornutum) and
Round-tailed Horned Lizards (P. modestum) consistently exhibited vigorous nest-site defensive behaviors (butting, open-mouth attacks, and biting
attacks) when experimentally approached in the field by a potential predator of reptilian eggs, Western Patch-nosed Snakes (Salvadora hexalepis).
During both prenesting and postnesting snake trials, such defensive attack behaviors by the female lizards were absent. Females of a viviparous
congener, Greater Short-horned Lizards (Phrynosoma hernandesi), failed to exhibit postpartum defensive behaviors to S. hexalepis, and newborns
did not associate in proximity to their mothers. Nest-site defense is suggested to be the ancestral behavior in the genus Phrynosoma, and it might
have been lost during the evolution of viviparity in certain species. Previous failures to detect nest defense behavior in Phrynosoma, and in related
clades of iguanian lizards, might be attributable to the absence of observations at nest sites after egg laying by such lizards, especially because
these behaviors occur only during brief time windows of potential nest detection by egg-hunting snakes. Similar trials with other iguanian lizards
and potential nest predators could reveal further examples of parental care in this diverse lineage of lizards.
Key words: Behavior; Greater Short-horned Lizard; Nest predation; Oviparous; Phrynosomatidae; Round-tailed Horned Lizard; Salvadora
hexalepis; Texas Horned Lizard; Viviparous

RECENT studies of selective forces involved in the
evolution of parental care have helped elucidate the
development of diverse systems of parental care in many
taxa (e.g., Clutton-Brock 1991; Royle et al. 2012). Although
parental care behaviors are widespread among fishes,
crocodilians, avian reptiles, and mammals, it is reportedly
rare in other reptiles such as chelonians and lepidosaurs
(lizards, 1.3%; snakes, 2.8%; Shine 1988; Greene 1999;
Greene et al. 2002; While et al. 2014). Reviews of the
occurrence of parental care in lepidosaurians suggest that
parental care could be any action by the parent after
oviposition or parturition that increases the chances of
survival of its offspring (e.g., Shine 1988). In lizards, the
behavior is almost unreported among the members of
Iguania, but it has been documented in clades of its sister
group, the Scleroglossa (Vitt and Cooper 1989; Greene 1999;
Somma 2003; Greene et al. 2006). Parental care is known
among members of the Pleurodonta (Iguanidae), but only
from five genera of large-bodied, mainly island-dwelling,
lizards where its expression might be limited to the
protection of nest sites by females from competing
conspecific females (Christian and Tracy 1982; Gibbons
and Watkins 1982; Wiewandt 1982; Shine 1988). Parental
care behaviors have not been reported in other lepidosaurian
clades, except possibly during nesting in tuataras (Shine
1988; Somma 2003), or postpartum agamids (Egernia; Qi et
al. 2012) and Xantusia (Davis et al. 2011).
Biologists interested in the evolution of life-history events
have attempted to use phylogenetic relationships to interpret
the significance of the expression or absence of parental care
in reptiles (Vitt and Cooper 1989; de Fraipont et al. 1996;
Blackburn 1999; Greene et al. 2006). There also remains
much to be learned from natural history data on parental
care in the various lineages and their homologies (Greene
1999; Shine and Lee 1999; Reynolds et al. 2002). The
1
CORRESPONDENCE: e-mail, wcs@amnh.org
majority of the literature is anecdotal and the potential
adaptive functions are conjectural (reviewed in Somma
2003). It is inappropriate to assume that taxa in which
parental behavior has not been reported actually lack the
behavior (Crump 1996; Somma 2003). Although it is
assumed that predation is the driving force that shapes
parental care, many studies are based on reactions toward
humans and few studies have demonstrated responses to
natural threats by predators (reviewed in Somma 2003; but
see Huang 2006, 2007; Huang and Wang 2009).
I performed field trials to determine whether gravid
females of two species of Horned Lizards (Pleurodonta:
Phrynosomatidae), Texas Horned Lizards (Phrynosoma
cornutum) and Round-tailed Horned Lizards (P. modestum),
might exhibit parental care. Females were followed to their
oviposition sites, and their patterns of remaining at these
sites were monitored. While at their nest sites, I examined
the female lizards’ responses to approach by the potential
nest predator, Western Patch-nosed Snakes (Salvadora
hexalepis; Degenhardt et al. 1996; Brennan and Holycross
2006). Salvadora hexalepis eat P. cornutum eggs (WCS,
personal observation). For comparison, behaviors of these
females were similarly tested before nesting and after they
had departed their nest locations.
This study addressed three questions: (1) Might females
remain at nest sites after oviposition and nest-site covering,
and if so, for what duration? (2) Would female lizards exhibit
any behaviors toward an S. hexalepis that might be
interpreted as defending their nests? (3) Might any such
defensive behaviors exhibited at nest sites differ from
behaviors exhibited by these females during similar snake–
lizard encounters at other locations before nesting, and after
females had departed their nest sites? If female Horned
Lizards (1) remain at their nest sites postoviposition; (2)
exhibit attacks against snakes that could consume their eggs;
and (3) do not exhibit such attack behaviors before nesting
and after nest-site departure, then these observations would
support the hypothesis that the lizards have a recognized

331
332 Herpetologica 73(4), 2017

TABLE 1.—Female Phrynosoma cornutum and P. modestum used in behavior trials with a potential predator (Salvadora hexalepis) during prenesting, at-
nest, and postnesting periods. The days at nest indicates the duration of the nest attendance before abandonment; the distance (m) from their nest site at the
time of the postnesting trials is also indicated.

Date of testing female lizards with snakes, and nest abandonment

Distance from nest
Subject no. Mass (g) Prenesting At-nest Abandonment Postnesting Days at nest for postnest trial (m)

P. cornutum
4 55.5 27 June 7 July 11 July 11 July 4 24
10 56.5 27 June 3 July 5 Julya 6 July 2 178
25 50.0 27 June 10 July 11 July 11 July 1 233
31 56.6 27 June 8 July 9 July 10 July 1 220
37 70.1 27 June 1 July 3 July 3 July 2 200
46 63.8 27 June 4 July 5 Julya 6 July 1 220
48 73.1 27 June 4 July 9 Julyb 9 July 5 250
52 58.0 (none) 27 June 29 June 30 June 2 164
P. modestum
4 14.7 28 June 3 July 5 Julya 6 July 2 24
10 8.2 28 June (predated)
20 17.2 30 June (lost)
a
Females observed at nest before heavy afternoon rain 5 July that had abandoned their nest by evening.
b
Female at nest 5 July that did not abandon nest.

form of parental care at nest sites. An absence of
observations of such behaviors would refute the hypothesis.
After revisions to the viviparous P. douglasii group
(Montanucci 2015), 11 of 21 Phrynosoma species are
viviparous (Leaché and McGuire 2006; Leaché et al. 2009;
Nieto-Montes de Oca et al. 2014). This trait appears to have
evolved twice in Horned Lizards (Montanucci 1987; Hodges
2004; Hodges and Zamudio 2004). To compare behaviors
among Phrynosoma species having different reproductive
modes, I asked similar questions about the responses of
viviparous Greater Short-horned Lizards (P. hernandesi),
after parturition: (1) Do recent postpartum females exhibit
any parental care behaviors? (2) Do newborn lizards remain
close to their mother, either before or after dark (sleeping)?
(3) In the presence of their offspring, do mothers attack a
snake predator (Stebbins 2003)? If attacks against a
predatory snake occur, and if neonates remain near their
mother rather than dispersing after parturition, these
behaviors would support the hypothesis of parental care.
An early report of parental care in P. hernandesi (misiden-
tified as P. cornutum; Lockwood 1883) describing a neonate
being protected by its mother was dismissed by Milne and
Milne (1950). Nevertheless, Milne and Milne (1950)
reported newborn P. hernandesi and mothers remaining
together.
MATERIALS AND METHODS
Subjects and Pretrial Conditions
Eight gravid female Texas Horned Lizards were collected
(23–29 May 2009) and three gravid Round-tailed Horned
Lizards were collected (24 May–8 June 2009) in Hidalgo Co.,
New Mexico, from highways (Sherbrooke 2002a). An
additional female P. cornutum (no. 52) encountered nesting
at the release study site 27 June 2009 was added to the study
(Table 1). Captive lizards were housed in large (3.8 3 7.0 3
2.4-m) walk-in outdoor enclosures (Sherbrooke 2008) at the
Southwestern Research Station (SWRS) of the American
Museum of Natural History, Portal, Cochise Co., Arizona.
Phrynosoma cornutum were liberally fed ants (Pogonomyr-
mex spp.) and domestic crickets (Acheta domestica; only
crickets for P. modestum), and all subjects had access to
water (Sherbrooke 1990, 2002b). All lizards gained mass
before release at the field study site (25 and 27 June for P.
cornutum and P. modestum, respectively). The study area, in
the San Simon Valley, Cochise Co., Arizona (30854.730 0 N,
109805.259 0 W; in all cases datum ¼ WGS 84; 1340 m in
elevation), is ~2 km south of a long-term ecological study
site (Brown et al. 1997). The Chihuahuan Desert vegetation
is dominated by shrubs, including Acacia, Ephedra, Flour-
ensia, Prosopis, and Yucca.
Before releasing lizards, PD-2 radio-transmitters (4–5 g;
Holohil Systems Ltd., Carp, Ontario, Canada) were attached
to six P. cornutum, and BD-2A radio-transmitters (1.5 g)
were attached to three P. cornutum and all three P.
modestum. Each radio-transmitter was coated with clear
100% silicone sealant and glued to the mid dorsum of a
subject (the exposed surfaces of each transmitter was lightly
coated with silicone and sprinkled with soil for camouflage).
Lizards were tracked using a Telonics TR-4 receiver
(Telonics, Mesa, Arizona) fitted with model RA-14K
antennae (Telonics). Lizards were located nearly daily
(sometimes twice daily), before nesting, at nest sites, and
after nesting. One P. cornutum (29 June) and one P.
modestum (9 July) were lost before nesting, and one P.
modestum was predated (10 July, apparently while nest
digging; Sherbrooke 2010). Because of these losses, field
trials at the nest site equaled nine for P. cornutum and one
for P. modestum. An additional at-nest trial was conducted
for a captive P. modestum. Air temperatures and rainfall
events were recorded.
Two Western Patch-nosed Snakes were collected in
Hidalgo Co., Arizona, where they are sympatric and
diurnally active with both Horned Lizard species (Sher-
brooke 2002a). The smaller and larger snakes’ snout–vent
lengths (SVLs), tail lengths, and masses were 44 and 52 cm,
10.5 and 13 cm, and 23.8 and 44.1 g, respectively.
Snake Trials Involving P. cornutum and P. modestum
Use of the two snakes was alternated throughout the field
trials. Snakes were hand-held in one of two clear-plastic
tubes (13 and 15 mm in diameter and 32 and 46 cm in
length, respectively, for smaller and larger snakes). The body
of each snake extended from both ends of the tube during
 SHERBROOKE—NEST-GUARDING BEHAVIOR
presentations to the lizard subject. The presenter restrained
the snake at the rear opening of the tube, thereby preventing
it from moving forward. About one-quarter of the anterior of
the snake’s body was able to move freely while the
experimenter, stooping, laying on the ground, or a combi-
nation, advanced the snake toward the subject. This
technique is similar to that used to elicit interactions
between snakes and Regal Horned Lizards (P. solare;
Sherbrooke and May 2008). The procedure was repeated
in each of the prenesting trails; at-nest trials (after egg laying,
after nest-hole filling, and after nest-site [camouflage]
covering); and postnesting trials (after desertion of nest
site), each of which were 3 min in duration. If lizards moved
from the original encounter site, the experimenter carefully
followed while advancing the snake throughout the trials. If
the lizard’s movements (long runs) suggested direct respons-
es to the snake and experimenter, the trial was terminated
early (after 30 s; in four prenesting trials only). Subsequent
responses by females, consistent with nest defense during at-
nest trials, indicated that even these shortened trials would
have elicited nest defense behaviors.
The presence of two or three people at the trial site
presumably, and sometimes obviously, influenced some
lizard behaviors. Human presence did not seem to affect
the behavioral consistency during each of the trial condi-
tions, especially where overt differences in responses by
females to the approaching snake were concerned. A
research assistant used a HandyCam HDR-XR500 (Sony
Corporation, Tokyo, Japan) to record the trials, except for
one prenest trial (lizard initially encountered nesting) and
one at-nest trial (trial opportunity was unanticipated with
only one person in the field). Field notes were recorded at
trial sites after each of 28 trials (10 prenesting, 9 at-nest, and
9 postnesting trials).
Analyses of the video recordings included counting the
number and form of attacks by the lizard on the snake
(rushed runs at the snake, often toward the head, resulting in
closed or open-mouth forceful collision or biting). Move-
ments by lizards away from the snake, or other defensive
behaviors were noted, such as body flattening and orienting
toward the threat, ‘‘dorsal-shield’’ displays, or head lowering
that enhances cranial horn visibility (Sherbrooke 1987, 1991,
2008, 2013; Sherbrooke and May 2008). Attacks by female
lizards consisted of forward lunges and runs at the snake,
ending in either butting, open-mouth pushing, or biting
(including pinching the skin for 1–3 s). Female subjects
sometimes missed hitting the snake because of poor
execution by the lizard or evasion by the snake.
Snake responses included apparent attempts to flee
(prevented by the presenter’s hold), sharp head and
forebody movements away from the lizard’s attacks, and
open- or closed-mouth strikes at the lizard. Repeated attacks
by a lizard on the snake often resulted in the snake’s location
being shifted away from the nest site. If this proceeded to ~1
m from the nest site, the female lizard would turn away from
the snake and walk back toward her nest. The presenter
holding the snake would then move it toward the nest to re-
engage the female. Dates of prenesting trials, at-nest trials,
nest abandonment, and postnesting trials were recorded, as
were number of days found at the nest, distances between
nest sites and sites for postnesting trials, and mass (g) of
gravid lizards (Table 1).
IN PHRYNOSOMA 333
On 23 May 2010, a single female Phrynosoma modestum
(SVL ¼ 64 mm; mass ¼ 16.1 g) laid 15 eggs (night of 28–29
May) in a circular fiberglass, open-top enclosure (123 cm in
diameter, 30 cm in height) within a large walk-in cage at the
SWRS (Sherbrooke 2008). The female was actively covering
the nest from 0715 to 0815 h when an S. hexalepis (also used
in 2009; SVL ¼ 45 cm, tail length ¼ 10 cm; mass ¼ 24.7 g)
was introduced into the enclosure and allowed to roam
freely. Interactions were video recorded. After the 15-min
trial and removal of the snake, the female lizard continued
surface nest-covering activities. The next day (0815 to 0830
h) the female was retested postnesting in the same
enclosure.
Snake Trials and Association Trials Involving P. hernandesi
Three gravid female Phrynosoma hernandesi (73, 73, and
74 mm in SVL and 29.8, 28.8, and 32.7 g in mass,
respectively) were collected in the Santa Catalina Moun-
tains, Pima Co., Arizona (32827.016 0 N, 110845.281 0 W; 2400
m in elevation), on 2 and 3 August 2010. While waiting for
parturition, lizards were maintained in the Tucson Moun-
tains west of Tucson, Arizona (793 m in elevation) in a
circular (122 cm in diameter, 67 cm in heighi) fiberglass-
walled, open-topped (partially shaded), sandy-soil floor
enclosure. These subjects were fed domestic crickets, and
water was available by means of mist-sprinkler cooling
systems that reduced midday temperatures in the enclo-
sures.
The first female to give birth (9 August; before 1030 h)
produced seven healthy young and one half-developed
aborted young (total mass ¼ 8.3 g; for the healthy young,
SVL ranged from 27 to 28 mm and mass ranged from 1.0 to
1.2 g), and she lost 13.3 g (41% of her mass). Nonbirthing
females were removed to a similar enclosure, and the mother
and her seven young were tested (1335 to 1400 h) with an S.
hexalepis (SVL ¼ 57 cm, tail length ¼ 16 cm; mass ¼ 41.3 g;
collected 26 June 2010 southwest of Tucson, Pima Co.,
Arizona). The snake was placed in the enclosure to wander
freely and video recordings were made of inter- and
intraspecific interactions. After removal of the snake, the
female (still within the fiberglass enclosure) was placed
within a smaller (43-cm-diameter) circular cage of hardware
cloth (pore size ¼ 12 mm2) through which she could not
pass, but her neonates could enter. After dark that evening,
the positions of the female and young were recorded.
On 14 August the second female gave birth (between
0900 and 1130 h) to eight young (total mass ¼ 8.4 g; neonate
SVL range ¼ 25–27 mm and mass range ¼ 1.0–1.1 g), and
she lost 12.8 g (44% of her mass). The third female gave
birth on 21 August (apparently before 1230 h) to 11 young
(total mass ¼ 9.0 g; neonate SVL range ¼ 24–27 mm and
mass range ¼ 0.7–0.9 g), and she lost 11.8 g (40% of her
mass). In both cases, after births, each female and her young
were left isolated within the enclosure and trials were
recorded when the S. hexalepis was introduced (1150 to
1300 and 1245 to 1420 h, respectively). In each of these two
trials, after removal of the snake, each female was left free
roaming with her young within the circular enclosure. The
proximity of the young to their mother was noted on several
occasions during the day, and distances of the juveniles’
sleeping locations from their respective mothers were
measured after dark. Nighttime location of juveniles was
334 Herpetologica 73(4), 2017

TABLE 2.—Gravid female Phrynosoma cornutum and P. modestum TABLE 3.—Female Phrynosoma cornutum and P. modestum behavioral
behavioral responses to Salvadora hexalepis during prenesting trials. A responses to Salvadora hexalepis during at-nest trials.
prenesting trial was not conducted for subject no. 52.
Lizard self-defensive and attack action
Air Snake action
Antipredator self-defensive action
Attacks on snake Subject no. temp (8C) Tongue licks Head lowered Dorsal-shield Strikes/bites Strikes lizard
Subject no. Air temp (8C) Run/walk away Head lowered Dorsal shield Strikes, bites
P. cornutum
P. cornutum 4 — 6 0 0 26 4
4 32.4 0 0 0 0 10 29.4 3 0 1 10 0
10a 31.4 4 0 0 0 25 28.8 4 0 1 10 10
25a 29.4 1 0 0 0 31 — 0 0 0 33 0
31 31.6 8 0 3 0 37a 31.0 — — — þ —
37a 28.0 2 0 0 0 46 30.8 2 0 0 23 10
46 31.0 0 3 4 0 48 33.0 3 0 0 49 12
48a 30.0 5 0 1 0 52 28.5 3 0 5 36 14
52 — — — — — P. modestum
P. modestum 4 29.0 0 0 2 42 0
4 28.9 0 2 4 0 a
Lizard no. 37, — indicates no video; þ indicates vigorous attacks on snake were noted.
10 33.0 0 3 0 0
20 28.2 0 1 3 0
a
Abbreviated trial times. postnesting presentations of the snake (Table 4). During
these trials (24 m from the nest), all females ran or walked
facilitated by late afternoon dusting their backs with UV away from the snake. During the period between nest
florescent powder and later use of an UV light source. abandonment and postnesting trials, females were followed
Postparturition trial times with these captive viviparous and never observed returning to their nest site.
lizards and free-roaming snake were longer (1 h) than the
3-min field trials with the oviparous species in which the Additional Captive P. modestum: At-Nest and Postnesting
snakes were hand held. This was done to ensure a sufficient Snake Trials
number of lizard–snake, close-contact encounters to fully There was no prenesting trial in captivity of the single P.
evaluate the lizards’ responses (both mothers and young). modestum in 2010. During the at-nest trial, this subject
attacked the snake, using open-mouth and biting behaviors
RESULTS throughout the trial; the snake bit back at the lizard. During
Prenesting Snake Trials (P. cornutum and P. modestum) its postnesting trial, still restricted to its nest site, this subject
The prenesting trials involving seven P. cornutum never attacked the snake, but it did exhibit several dorsal-
females, 2 days after release, occurred 4–13 days before shield defensive behaviors.
the at-nest trials; female no. 52 was captured while nesting
and therefore lacks a prenesting trial (Table 1). The gravid Behavioral Comparisons Among Trial Types
female P. modestum pretrial dates were 1–3 days after In P. cornutum, there were significant differences
release, and the single female that continued in the study between attack frequency among the different trial types:
was pretrial tested 5 days before nesting (Table 1). During Prenesting trials (zero attacks and seven no-attacks; binomial
prenesting trials, no gravid female P. cornutum (n ¼ 7) or P. P ¼ 0.008), at-nest trials (eight attacks and zero no-attacks;
modestum (n ¼ 3) exhibited any attacks on the snake (Table binomial P ¼ 0.004), and postnesting (zero attacks and eight
2). Five of seven P. cornutum ran or walked away from the no-attacks; binomial P ¼ 0.004; Zar 1984). The occurrence of
snake, one head lowered (horns raised), and three displayed attacks during prenesting trials differed significantly from
dorsal shields (Note: four trials with abbreviated-trial times that during the at-nest trials (sign test P ¼ 0.008). A similar
were scored as no attacks; Table 2). No P. modestum moved pattern was detected when comparing the occurrence of
away from the snake, and all females lowered heads and two attacks during the at-nest and postnesting trials (sign test P ¼
displayed dorsal shields in response to the snake’s activities. 0.004; Zar 1984). Attack or no-attack responses in the few
trials with P. modestum were similar to P. cornutum. Only
At-Nest Snake Trials (P. cornutum and P. modestum)
During all at-nest trials with both P. cornutum (n ¼ 8) and TABLE 4.—Female Phrynosoma cornutum and P. modestum behavioral
P. modestum (n ¼ 1), female attacks on the snakes involved responses to Salvadora hexalepis during postnesting trials.
head-butting, open-mouth strikes, and bites often aimed at
the snake’s head (Table 3). During these attacks the snakes Antipredator self-defensive action
Attacks on snake
responded with strikes at the lizard in five of seven recorded Subject no. Air temp (8C) Run/walk away Head lowered Dorsal shield Strikes, bites
P. cornutum at-nest trials, but not in the P. modestum trial. P. cornutum
Six of seven recorded responses of female P. cornutum 4 30.0 8 0 0 0
involved tongue licks of the snake’s skin, not seen in the P. 10 27.8 9 0 1 0
modestum trial. No females exhibited head lowering (raising 25 28.8 9 0 0 0
31 28.9 7 0 2 0
horns), but dorsal shields were displayed by three of seven P. 37 29.1 3 0 1 0
cornutum and the P. modestum. 46 26.4 4 2 3 0
48 30.6 6 2 2 0
Postnesting Snake Trials (P.cornutum and P. modestum) 52 27.0 4 1 3 0
None of the female P. cornutum (n ¼ 8) and P. modestum P. modestum
4 24.0 4 1 3 0
(n ¼ 1) exhibited any attacks on the snakes during
 SHERBROOKE—NEST-GUARDING BEHAVIOR
two female P. modestum received at-nest trials (one in 2009,
one captive in 2010), and both attacked the snake. Three
lacked attack responses in prenesting trials, and two also
failed to attack in postnesting trials (one in 2009, one captive
in 2010).
Observations from Trials Involving P. hernandesi
None of the postpartum female P. hernandesi attacked
the snake, nor did the snake attack any of the neonate or
adult female lizards. In all three trials, there were close
encounters between the adult lizard and the snake (seven to
nine per trial), often with physical contact (one to six per
trial). These females never ran toward or away from the
snake. In two trials, the female never moved from her
original position throughout the trial. Females often
responded to close snake approaches or contacts with head
depressed postures, or body raising and tilting of the back
slightly toward the passing snake (dorsal shield). The snake
occasionally tongue flicked and generally seemed to seek
escape from the enclosure throughout each trial.
During daytime observations of the neonate lizards with
their mothers, no tendencies for them to associate with the
females were noted. At night, in the first trial four of seven
young were located on the surface at approximate distances
of 30, 35, 65 and 70 cm from the female; others were buried.
During the second trial, two of eight neonates were on the
surface (distances to the mother ¼ 15, 32, 63, 65, 95, 100,
110, and 116 cm); during the third trial, 7 of 11 neonates
were on the surface (distances to the mother ¼ 0, 34, 38, 39,
45, 67, 70, 80, 104, 106, and 110 cm). Among the 23
hatchlings located, only one was in contact with its mother
when sleeping, on her back at the edge of the enclosure.
DISCUSSION
Gravid females of two size-dissimilar species of oviparous
horned lizards (Table 1; Sherbrooke 2003) consistently
exhibited defense of their nests when presented with an
egg-eating snake in every at-nest trial. These same subjects
never exhibited these behaviors during prenesting or
postnesting trials. These data support the conclusion that,
during the period immediately after nesting when females
attend their nest, they defend those sites against snakes that
might burrow into the nest and depredate their eggs.
Shine (1988) listed four categories of parental care by
female squamates: (1) female defends nest site briefly against
conspecific females; (2) female coils around eggs, defending
against predators and possibly elevate nest temperature; (3)
female remains with eggs after deposition and might defend
them against predation or pathogens; and (4) female aids
newly born/hatched young. The female nest site defense
against an egg-eating snake by P. cornutum and P. modestum
reported here incorporate aspects of two of these categories,
but they are not adequately described by either. Category 1
female nest defense is not present among the species tested.
With category 3, horned lizard females do not remain with
the eggs for their defense but defend the site, having buried
their eggs to incubate for a duration (~60 days) that extends
considerably beyond the period of nest site defense. Shine
(1988) focused his discussion of egg brooding on thermal
aspects of egg attendance, and egg guarding on active nest
defense against predators, a rare event. The observations of
IN PHRYNOSOMA 335
the present study indicate nest-site defense against snake
predation during an initial period of incubation, followed by
nest-site desertion after several days. These nest-defending
behaviors are a form of parental care that could enhance
reproductive success. Apparently these parental care behav-
iors are innate. Further studies could determine whether
behavioral shifts between prenesting and at-nest, and
between at-nest and postnesting, are influenced by changes
in hormone levels or other chemical signals from the eggs.
The cost to females of this parental care might be minimal
and the benefits significant (Huang 2007). The risks for
female horned lizards of engaging in nest defense against a
guild of small egg-eating snakes may be minimized by these
snakes generally being restricted in girth and gape, by female
horned lizards consistently being the larger sex (Zamudio
1998), and by the presence of their cranial horns. Nest
attendance after oviposition (periods of 1–5 days; Table 1)
might restrict feeding or access to shade and nocturnal
retreats (Sherbrooke 2003, 2013), but ant feeding, use of
shade under shrubs, and shrub climbing at night by at-nest
females were all recorded (WCS, personal observation).
Why might this brief postegg-laying nesting period be
critical for parental-care nest defense? I hypothesize that
reptile egg–eating snakes use chemical scents exuded during
egg laying to locate nests and that these scents dissipate over
several days, thus negating the need for longer-term nest
guarding. My observations include a light rain event
overnight on 4–5 July, followed by heavy precipitation
between 1730 and 1830 h on 5 July. Three female P.
cornutum and one P. modestum were at their nest sites
during that morning (0730 to 0830 h), but three of these
females had abandoned their nest sites by evening (1830 to
1930 h; Table 1). Perhaps females are aware of changes in
chemical signals at nest sites, including decreases that follow
precipitation, in making nest-site abandonment decisions;
alternately, females might respond directly to significant
rainfall.
Huang (2006) showed that Mabuya longicaudata females
distinguished between an egg predator and a lizard predator
and that they might adjust their duration of nest attendance
in response to nest discovery by egg-eating snakes. Because
P. cornutum and P. solare respond differently and appropri-
ately to threats from different snake predators (Sherbrooke
2008; Sherbrooke and May 2008), specific types of threats
might be recognized by horned lizards. Also, female licking
of snake integuments during at-nest trials suggests that they
might evaluate threats of different snakes via chemical cues
(Bealor and Krekorian 2002; Kabes and Clark 2016). The
combined use by nesting female horned lizards of nest-
defense attacks with antipredator self-defense behaviors
during at-nest trials suggests mixed behavioral responses of
the females during their nest defense. Perhaps the relative
size differences between the females of different species and
their predators would produce different frequencies of
expression of these behaviors. Nest defense against non-
reptilian potential egg predators remains unexplored.
Trials with the postpartum P. hernandesi did not produce
any aggressive behaviors toward the snake. Parental care
seen in some oviparous species might not occur in some
viviparous species of horned lizards. The scattered distribu-
tion of juveniles in the enclosure, regardless of time period,
suggests no postpartum attachment of juveniles to their
336 Herpetologica 73(4), 2017
mothers. Because the births and trials were conducted in
restrictive conditions of captivity, these data might not be
sufficient to rule out parental care by viviparous species of
horned lizards. Postpartum affiliation of neonates and their
mothers, for parental care, is known in several genera of
crotaline snakes (Greene et al. 2002). Further field-based
observations are needed to resolve issues of postpartum
parental care in the lineages of viviparous horned lizards.
Nest-defense behaviors in female P. solare were similarly
studied in Pima Co., Arizona (WCS, personal observations).
The pattern and intensity of nest defense during at-nest trials
among these females was similar to that reported here for P.
cornutum and P. modestum. As such, these behaviors might
be widespread among members of the genus Phrynosoma.
This conclusion is further supported by observations of nest-
site tenacity after egg deposition in Phrynosoma asio
(Garcı́a-Pareja 2012; M. Garcı́a-Pareja, personal communi-
cation). Further studies to expand observations on P.
modestum and other oviparous species are warranted.
Recent phylogenetic analyses of horned lizards (Leaché
and McGuire 2006; Nieto-Montes de Oca et al. 2014) have
resulted in the designation of four clades, two of oviparous
species and two of viviparous species. There are two basal
tree species, P. cornutum and P. asio—both of which might
guard their nests. Phrynosoma modestum is in the Dolio-
saurus clade and P. solare is in the Anota clade, suggesting
possible widespread occurrence of nest-guarding parental-
care behaviors among egg-laying species. Phrynosoma
hernandesi, which seems to lack postpartum parental
behaviors, is in the Tapaja clade. Indeed, if such behavior
is lacking in this species and its close relatives, and it has
been lost during the evolution of viviparity in this clade,
another possibility to evaluate the loss of nest-guarding
parental-care behaviors during the evolution to viviparity
might be found in the Brevicauda clade.
The paucity of reports of parental care in iguanian lizards
might reflect the rarity of this behavior type, a failure to
detect its presence, or a lack of observations under
appropriate conditions for interpretation (i.e., being at nest
sites when threatened by an egg predator). Behaviors of
female P. cornutum lingering at nest sites have been
reported (e.g., Sherbrooke 2002c; Allison and Cepeda
2009, 2010), but they were not connected to possible nest-
guarding parental care. The findings reported here suggest
that further studies of parental care in other genera of
phrynosomatids, and other clades in the Pleurodonta, are
worth pursuing.
Acknowledgments.—I thank S.W. Sherbrooke and R.C. Sherbrooke for
field assistance, W.E. Cooper, Jr., for statistical assistance, and J.E.
Ambrose, Jr., for Spanish translation assistance. Collecting permits were
provided by Arizona Game and Fish Department (SP746072, SP594729)
and New Mexico Department of Game and Fish (1149). Trial procedures
and animal care followed American Museum of Natural History Institutional
Animal Care and Use Committee protocol, and the staff and volunteers at
the Southwestern Research Station facilitated studies.
RESUMEN: Este es el primer informe de defensa
contra depredadores al nido por lagartos iguania.
Hembras de Camaleones Com ún (Phrynosoma
cornutum) y Tapayaxin (P. modestum) mostraron
conductas defensivas consistentes y vigorosas al sitio
del nido (cabeceadas, choques con boca abierta, y
mordeduras) cuando experimentalmente se acercó en
el campo por un depredador potencial de huevos de
reptiles, Salvadora hexalepis. Durante ensayos de
serpientes, tanto en sitios pre- y post-anidación, tales
conductas defensivas de ataque por parte de los
lagartos hembras eran ausentes. Hembras de un
congénere vivı́paro Camaleón con Cuernitos de
Monta ña (Phrynosoma hernandesi) no exhiben
comportamientos defensivos post-parto a S. hexalepis,
y las crias recién nacidos no se asociaron con sus
madres. Defensa de sitios de nidificación se sugiere
que es el comportamiento ancestral del género
Phrynosoma y puede haber sido perdido durante la
evolución de la viviparidad en ciertas especies. Los
fracasos anteriores para detectar el comportamiento de
defensa de nido en Phrynosoma, y en otros clados de
lagartijas iguanian, puede ser debido a la falta de hacer
observaciones al nido después anidación de tales
comportamientos lagartijas, especialmente porque
estos comportamientos ocurren sólo durante breve
tiempo de potencial nido-detección por serpientes que
cazan huevos reptil. Ensayos similares con otros
lagartos iguanian y predadores potenciales del nido
pueden revelar más ejemplos de cuidado parental en
este diverso linaje de lagartos.
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Accepted on 16 August 2017
Associate Editor: Chris Gienger