Behaviour (2021) DOI:10.1163/1568539X-bja10065 brill.com/beh

Maternal care and secretive behaviour of neonates in the highly social lizard Liolaemus leopardinus (Squamata: Liolaemidae) from the central Chilean Andes may relate to size-specific bird predation
Enrique Santoyo-Brito a,∗, Susana Perea-Fox b , Herman Núñez c and Stanley F. Fox a
a Department of Integrative Biology and Collection of Vertebrates, Oklahoma State University, Stillwater, OK 74078, USA b Department of Languages and Literatures, Oklahoma State University, Stillwater, OK 74078, USA c Area Zoología, Museo Nacional de Historia Natural de Chile, Santiago, Chile *Corresponding author’s e-mail address: enrique.s.brito@okstate.edu
Received 6 May 2020; initial decision 28 July 2020; revised 19 December 2020; accepted 28 December 2020
Abstract
Predation prompts the evolution of antipredator traits, molds behaviour, and can lead to the evolution of parental care. We investigated parental care and predator-avoidance behaviour of neonates in the social lizard Liolaemus leopardinus. We used clay models to quantify bird predation pressure on L. leopardinus. Predation was significantly greater on small models and models in open habitat. Late-term pregnant females left their social groups on rock outcrops and gave birth in solitary underneath flat rocks in vegetated microhabitat. Mothers stayed with their litters inside natal chambers for at least 24 h and when they left, sealed the neonates inside. Mothers remained close to their natal chamber and neonates when neonates emerged. Neonates and young yearlings moved significantly less and occupied vegetated microhabitat significantly more than older age classes. We suggest that the maternal behaviour and secretive behaviour of neonates may be related to the heavy avian predation on neonates.
Keywords
anti-predation, birds, clay models, group living, parental care, reptile.
© Koninklijke Brill NV, Leiden, 2021
DOI 10.1163/1568539X-bja10065

2 Behaviour (2021) DOI:10.1163/1568539X-bja10065
1. Introduction
Predation is a selective force that molds behaviour and prompts the evolution
of antipredator traits, for example, nest guarding, direct repulsion, startle
response, crypsis, etc. (Krebs & Davies, 1993; Lanham & Bull, 2004; Huang
& Pike, 2011; Davies et al., 2012). Among those traits, cryptic colouration
(i.e., background matching) and cryptic behaviour (i.e., remaining still or
moving little; Cooper et al., 2008; Webster et al., 2009; Vignieri et al., 2010;
Stevens & Ruxton, 2019) are two very effective techniques animals use to
avoid visually oriented predators (Lima & Dill, 1990; Capodeanu-Nägler et
al., 2016). Animals may also reduce predation pressure through a shift to
safer habitats (Dickman, 1992; Pierce, 1998; Winandy et al., 2016). This
strategy is especially important for juveniles since small, young conspecifics
tend to have more predators than their adult counterparts (Reznick, 1996;
Costelloe & Rubenstein, 2015). This disproportionate predation pressure
decreases over time as young individuals achieve a certain size threshold as
shown in amphibians (Caldwell et al., 1980; Smith, 1983), mammals (Longland
& Jenkins, 1987), fishes (Reznick, 1996) and crustaceans (Moksnes et
al., 1998).

Strong predation pressures can also lead to the evolution of parental care,
defined here as any form of behaviour expected to increase the successful
production of progeny (Clutton-Brock, 1991; Balshine, 2012; Smiseth et al.,
2012). Parental care has evolved independently in a broad range of taxa,
and has been well documented in mammals and birds, groups in which
the behaviour prevails through long term parent-offspring associations and
social interactions. Interactions like burrow or nest sharing and nutritional
provisioning promote parent-offspring associations and make parental care
possible (Clutton-Brock, 1991; Costelloe & Rubenstein, 2015).
It has long been thought that reptiles lack sociality and, consequently, lack
parental care (Somma, 2003a; Balshine, 2012; Doody et al., 2013; While et
al., 2014). However, parental behaviour has been described in more than 140
reptile species of the more than 9500 known living species (Somma, 2003a,
b; Huang, 2006; Doody et al., 2013 and references therein). Therefore, it is
plausible that many more yet undocumented cases of parental behaviour in
reptiles exist. Reptile parental behaviour is mainly expressed in rather simple
forms (e.g., guarding or defense of nests/burrows, eggs, or offspring;
Somma, 2003a; Huang, 2006; While et al., 2014). Nevertheless, complex
E. Santoyo-Brito et al. / Behaviour (2021) 3
forms and degrees of parental care have been described for the group, especially
in relatively long-lived lizard species (Gans, 1996; Chapple, 2003;
Balshine, 2012; Doody et al., 2013). Research on parental care of squamate
reptiles (lizards and snakes) is still in its early stages (While et al.,
2014). Many species of reptiles are elusive and secretive, making it difficult
to locate their oviposition and birth sites, therefore parent-offspring associations
and parental behaviour are challenging to observe and document in-situ
(While et al., 2014). Thus, in many instances, contributions to our knowledge
of parental behaviour in reptiles are anecdotal observations (Lemos-Espinal
et al., 1997; Masters & Shine, 2003; Rismiller et al., 2010; While et al.,
2014). Despite these shortcomings, reptiles serve as a good general model
for discerning the selection pressures that develop parental care and drive its
complexity because parental care is not as predominant as in fish, birds and
mammals; parental care in reptiles, especially lizards, is only now emerging
as an important natural history trait (While et al., 2014).
Liolaemus leopardinus (Müller & Hellmich, 1932) is a medium-to-large
lizard endemic to temperate central Chile. The geographic range of the
species is limited to a narrow altitudinal band above timberline at 1800–
3000 m (Pincheira-Donoso & Núñez, 2005; Pincheira-Donoso et al., 2008).
Low temperatures and seasonal scarceness of resources are characteristic
of the habitat. Lizards are active during austral spring, summer, and fall,
and inactive during the extreme austral winter. Individuals of the species
are long-lived and their life span can exceed a decade (Santoyo-Brito et
al., 2018). The species is highly social; at times groups on rock outcrops
are formed by two adults (male and female) and one to three juveniles
(Fox & Shipman, 2003), and at other times larger groups of up to 6–10 (or
more) adults and juveniles on open rock outcrops and within crevices are
observed (Santoyo-Brito, 2017). Despite their cryptic colouration, individuals
basking or moving on the open rock are relatively conspicuous. High
genetic relatedness among individuals within these social groups is common
(Santoyo-Brito, 2017). Although pregnant females are sometimes found
within the social groups, results of a pilot study conducted in 2005 indicated
that neonates are not found within the groups; we again observed this during
two field seasons in the late spring and summer of 2011–2012 and 2012–
2013 (Santoyo-Brito, 2017). Female L. leopardinus appear to reproduce on
a yearly basis, giving birth to only 2–4 neonates (Santoyo-Brito et al., 2017).
4 Behaviour (2021) DOI:10.1163/1568539X-bja10065
At the high elevations where L. leopardinus lives, visually oriented predators
that prey on lizards (especially smaller individuals) are two abundant
species of shrike-tyrants, Agrionis montana and Agrionis livida, the less
abundant American Kestrel, Falco sparverius (Ridgely & Tudor, 1994), and
the very common Rufous-banded Miner, Geositta rufipennis (Santoyo-Brito
et al., 2014). During March-April, when females give birth, A. montana,
A. livida, and G. rufipennis are abundant at El Colorado, our study site in
central Chile. Thus, bird predation on small neonate L. leopardinus appears
to be intense (Santoyo-Brito et al., 2018). Another potential predator is the
saurophagous snake Tachymenis chilensis (Greene & Jaksic, 1992). At our
high-elevation site, however, T. chilensis is very rare and likely has minimal
impact on total predation pressure. Likewise, cannibalism by larger L. leopardinus
or predation by sympatric lizard species L. bellii and L. nigroviridis
have not been reported and can probably be ruled out. Therefore, we suggest
that high predation risk by visually oriented birds has caused neonates
to seek more vegetated, protected habitat than the open habitat where the
conspicuous social groups of the species live. A similar ontogenetic shift in
habitat use has been reported in crayfish, fish, birds, and mammals. Young
individuals inhabit a more protected habitat when compared to the open habitats
occupied by adults (Laegdsgaard & Johnson, 2001; Gow & Wiebe, 2014;
Costelloe & Rubenstein, 2015; Dyer et al., 2016).
During the austral fall of 2012 at our study site in central Chile, we
employed clay lizard models to quantify the predation pressure on individuals
of different size classes of L. leopardinus. We hypothesized that avian
predation would be stronger on models representing the neonate size class
than on older juvenile and adult size classes, and predation would be weaker
on those models under cover than in the open. If true, it is possible that
strong size-specific predation pressure has favored L. leopardinus to evolve
parental care (e.g., in the form of nest selection, placement of neonates in
more protected microhabitat, and active protection against predators). We
radiotracked pregnant mothers to document their movements and habitat use
before and after giving birth and to locate birthing locations, and we used
a flexible borescope to observe the mothers with their offspring inside natal
chambers. Strong size-specific predation may also force neonates to both
behave secretively and utilize a microhabitat secluded from large open rock
outcrops where they would be more susceptible to predation by visual predators.
This secretive behaviour of neonates might explain why no neonates
E. Santoyo-Brito et al. / Behaviour (2021) 5
have ever been reported from the field. Such secretive and cryptic behaviour
would be expected to be retained until the neonates attain a greater size, making
them less susceptible to predation, just like in crayfish, tadpoles, fish,
birds, and others (Stein & Magnuson, 1976; Caldwell et al., 1980; Smith,
1983; Reznick, 1996; Grol et al., 2014; Hoy et al., 2014). To document the
proposed secretive neonate behaviour and how it changes with age, we used
radiotelemetry to quantify neonate movements and habitat use, and compared
that to adults and older juveniles at the same time of the year, and also
compared movements and habitat use of 7–8 month-old juveniles early the
next spring to that of adults and older juveniles then.

2. Materials and methods
Our study was conducted in the Andean cordillera of central Chile at El
Colorado, 35 km northeast of Santiago at 2760 m (33°14S, 70°16W; Fox
& Shipman, 2003; Santoyo-Brito, 2017). The climate is characterized by dry
summers, snowy austral winters, and a Mediterranean pattern of rainfall (di
Castri & Hajek, 1976). The bare rock outcrops characteristic of our study site
are located in treeless habitat dominated by patches of dwarf shrub Berberis
sp. Liolaemus leopardinus shows little sexual size dimorphism, although
adult males (mean Snout-Vent Length (SVL) = 100.8 mm) are slightly larger
than adult females (mean SVL = 99.6 mm; Fox & Shipman, 2003; Santoyo-
Brito et al., 2018). Free-ranging neonates are much smaller (N = 6; mean
SVL = 40.9 mm).
In austral fall (mid-March of 2012), we estimated predation pressure from
placement of 108 clay models of three size classes (neonate, juvenile, and
adult; N = 36 models/size class) in three microhabitats (open rock faces,
open soil, and under bushes; N = 36 models/microhabitat) for four days for
a total of 432 model days. All three microhabitats were commonly used by
lizards. Snout-vent length of each size class (40, 60, and 90 mm SVL, respectively)
was determined from a pilot study conducted in 2005 and from Fox &
Shipman (2003). Models were made of one hatchling Crotaphytus collaris,
and one juvenile and one adult L. leopardinus deposited at the Collection of
Vertebrates (COV) at Oklahoma State University prior to our fieldwork in
Chile. At the time, we did not have access to neonates of the species, and
hatchlings of C. collaris are similar in body size and morphology to L. leopardinus
at this young age. Lizard specimens were arranged in a basking position
and covered with silicone (Dragon Skin® Series; Smooth-On, Macungie,
6 Behaviour (2021) DOI:10.1163/1568539X-bja10065
Figure 1. Comparison of a live lizard and typical model made with custom-mixed modeling
clay to estimate predation pressure of three size classes (neonate, juvenile and adult) of
Liolaemus leopardinus during mid-March of 2012 at El Colorado, Chile.
PA, USA). Once hardened, the silicone was cut open and the lizard removed,
leaving a detailed inverse mold. Molds were filled with custom-mixed modeling
clay matching the background colour of the lizards, and after removal
of the models, black dots and a line resembling the dorsal vertebral line were
painted over the body to match the colour pattern of live animals (Figure 1).
To prevent predators from carrying away the models, models were tied to
a bush or rock in the appropriate microhabitat using a clear monofilament
fishing line. Models were placed 3 m or more from each other. We also used
six camera-traps (2 Stealth Cams, GSM Outdoors, Grand Prairie, TX, USA,
and 4 Moultrie Bird Cams (Models WSCA02 and 03), EBSCO Industries,
Birmingham, AL, USA), each one placed at an approximate distance of 1 m
from six different clay models (2 of each model size) located in either open
soil, open rock, or under vegetation. The camera (set to high sensitivity for
motion triggering) was positioned horizontally at substrate level or above
E. Santoyo-Brito et al. / Behaviour (2021) 7
the model using a tripod. The camera was used to document the species that
made attacks and time of attack.
To document the pre- and postpartum behaviour of pregnant females during
our second field season, we attached radio-transmitters (model: BD-2H,
0.9–1.04 g, internal antenna; Holohil Systems, Carp, ON, Canada) to the tail
base of nine adult pregnant females. During late December to early April,
we attempted to radiolocate all radio-tagged subjects at least two times a
day from approximately 10:00 am to 6:00 pm. In late April of 2013, we fortuitously
captured two free-ranging neonate L. leopardinus; this presented
us with the opportunity to glue a miniature radio-transmitter (model BD-2x,
11.5 by 5.3 by 2.8 mm; 0.25 g, external antenna; Holohil Systems) to the
dorsum of each one to study their behaviour. In November 2013 (early
austral spring) we revisited our field site to capture and radio-tag three 7–
8-month-old juveniles (hereinafter young yearlings) with the same model
of radios (data on radiotelemetry in Table A1 in the Appendix). To locate
all radio-tagged subjects, we used a hand-held, three-element Yagi antenna
and a radio-receiver (Model R-1000; Advanced Telemetry Systems, Isanti,
MN, USA). When the subject (mother, neonate, or young yearling) was
radio-located underneath a rock or within a rock crevice, we removed the
co-axial cable from the antenna and used that end of the cable to pinpoint the
exact location. To observe and video-record behaviour of refuged lizards, we
used a Rigel digital video borescope (Medit, Winnipeg, MB, Canada) with
a 360-degree, two-way articulating probe (4 mm in diameter and 2 m long).
All lizards were part of an intensive, two-year behavioural study. Thus, in
addition to the radio-transmitter on a subset of lizards (N = 15), all subjects
(N = 62) were permanently marked by both a unique toe-clip and a dorsal
colour code combination of non-toxic latex paint dots, which allowed recognition
of individual lizards from a distance without the need for recapture.
Lizards were initially captured via noosing, SVL measured with a ruler, and
sex determined by the presence (males) or absence (females) of precloacal
pores when a hemipenal bulge was not observed (Santoyo-Brito et al., 2018).
On our study site, we placed scattered, numbered flags on top of prominent
rocks, which could be seen from a distance. The location of each flag
was recorded using a handheld GPS (Datum WGS84). We used this geographic
information to create scale maps of our study site, implementing
ArcMap v10.1. Maps were ground-truthed in the field and adjusted when
8 Behaviour (2021) DOI:10.1163/1568539X-bja10065
needed. We collected spatial data of marked L. leopardinus by visual sightings,
capture and recapture of lizards when necessary (e.g., subject missing
paint dot colours), scan sampling (focal observation via binoculars; Frost
& Bergman, 2012), and radio-transmitter locations (attached to pregnant
females, neonates, and young yearlings; data in Table A1 in the Appendix).
To do this we walked slowly through the study area while recording the spatial
location of marked lizards on a hardcopy map of our study site. The
flags aided us to position the location of sightings to ±1 m by triangulation.
Spatial data collection took place from approximately 10:00 am to 6:00 pm.
It is not likely that our activities on the study site influenced the behaviour
of the lizards. During radio-tracking surveys, the radio signal (i.e., beeping
sound) of the radio-transmitters attached to subjects could be detected
by the radio-receiver as far away as 60–70 m, but more commonly at 30–
40 m even when radio-tagged individuals were in crevices 10–28 cm deep
(Santoyo-Brito & Fox, 2012, 2015). The signal increased in strength as the
antenna and receiver got closer to the radio-transmitter. The signal combined
with our constant scan sampling in the direction of the strongest signal aided
us to locate known individuals from a distance, making it unlikely that the
lizard position was influenced by our presence. We also know that maximal
distances of radio-signal detection exceeded by far the distance at which L.
leopardinus seeks refuge when threatened by a human simulating a predator
(Santoyo-Brito et al., 2020). The observed individuals were never intentionally
flushed to seek refuge.
From late March through April 2015, we measured temperatures of the
microhabitat underneath flat rocks similar to natal chambers during night
(8:00 pm to 6:00 am) and day (10:00 am to 6:00 pm). We placed 8 pairs of
iButtons (iButtonLink, Whitewater, MI, USA), one of each pair underneath
a flat rock and the other underneath a nearby bush and recorded temperatures
once an hour for 41 days.

2.1. Statistical analyses
To analyze predation pressure from placement of clay models, we used loglinear
models in Multiway Frequency Analysis (MFA) that included model
size, microhabitat, and attack frequency to calculate and test for significant
two-way associations in the data. In this MFA, we pooled adjacent categories
in the contingency table so as not to violate the assumptions of the analysis:
no more than 20% of expected values less than five and no expected
E. Santoyo-Brito et al. / Behaviour (2021) 9
value less than one (Tabachnick & Fidell, 2013). We pooled medium and
large lizard models and compared them to small ones as our size variable
(because our hypothesis was that small models would sustain more attacks
than larger ones), and pooled the open microhabitats of rock and ground and
compared them to the closed microhabitat of beneath bushes as our microhabitat
variable (because our hypothesis was that models in the open would
sustain more attacks than those under protective cover). Our resulting binary
variables of model size, microhabitat, and attacked or not did not violate the
MFA assumptions.

To compare the distances moved by different age classes of lizards, we
first determined the average distance between consecutive locations of each
marked lizard using the Haversine formula to calculate the linear distance in
meters (Curry, 2014; Taylor et al., 2019). Because we had too few neonates
and young yearlings to perform traditional statistical analyses, we used
randomization tests (1000 iterations) to evaluate (1) differences between
neonates and adults/juveniles and (2) differences between young yearlings
and adults/juveniles in the average distance between consecutive locations.
We first calculated the mean distance between consecutive locations for all
neonates or all young yearlings, then counted the number of times out of
1000 iterations the mean of the same number of subjects pulled randomly
from the set of adults and juveniles was equal to or smaller than the mean of
the neonates or young yearlings. A count less than 50 was considered statistically
significant, with the conclusion that the neonates or young yearlings
moved less.

To test for statistical difference in habitat (i.e., off and on open rock outcrops)
of 1) neonates versus adults/juveniles, and 2) young yearlings versus
adults/juveniles, we used in each case a χ2 test of independence of number
of locations of lizards in the two habitats. For both the randomization and
the chi-squared tests, we limited the analyses to the spatial data recorded
during March-April and November-December. These are the months when
adults/juveniles and neonates, and adults/juveniles and young yearlings,
overlap, respectively.

To compare the locations of known mothers in relation to the respective
natal chamber of each for the prepartum, parturient, and postpartum time
periods, we tallied the number of sightings less than and greater than 5 m
from each mother’s natal chamber in each time period (all days before giving
birth (prepartum), birth day plus five days (parturient), and all days after the
10 Behaviour (2021) DOI:10.1163/1568539X-bja10065
six-day parturient period (postpartum)) for each mother. We pooled counts
of the three mothers less than and greater than 5 m from each mother’s natal
chamber and performed an overall Chi-squared test of heterogeneity across
the three time periods. To test if individual mothers showed non-random
proximity to the natal chamber across the three time periods, we conducted
a randomization test. We made 1000 iterations of randomly scrambling all
of each mother’s distances from the natal chamber and randomly placing
them into the three time periods, retaining the respective sample sizes of
sightings for each mother in each time period, and tallied the number of
times all three mothers changed their behaviour as did the three mothers over
the actual three time periods, i.e., how many times over the 1000 iterations
did randomized sightings of all three mothers show a decrease in distances
from prepartum to partutient and an increase in distances from parturient
to postpartum. A count less than 50 was considered statistically significant,
with the conclusion that individual mothers followed the same pattern over
the three time periods observed for mothers’ sightings combined.
To analyze the late fall temperatures below flat rocks and within nearby
bushes and to ensure that we did not inflate the sample size by pseudoreplication,
we first averaged the maxima of all the hourly day and nighttime
readings over the 41 days of data collection for each iButton and then used
paired t-tests to compare the mean maximal temperatures under a rock and
within a bush for the day and night intervals. Before conducting the paired
t -test, we tested if the distributions of paired differences were normal with
the Kolmogorov-Smirnov test. We performed all statistical analyses using
SPSS (v21.0, IBM, Armonk, NY, USA).

3. Results
Small clay models were attacked more often and medium and large clay
models less often than expected by chance (Table 1). Models in the open
(rock and ground) were attacked more often and those under bushes less
often than expected by chance (Table 2). The two-way association of size
and attack frequency (partial χ2 = 7.86, df = 1, p = 0.005) and of microhabitat
and attack frequency (partial χ2 = 12.05, df = 1, p = 0.001) were
statistically significant. There was no significant association of size and
microhabitat (partial χ2 = 0.85, df = 1, p >0.05). Marks left on the models
indicated bill strikes from predatory birds. We observed large numbers of the
E. Santoyo-Brito et al. / Behaviour (2021) 11

Table 1.
Clay models, by size, attacked by birds during mid-March of 2012 at El Colorado, Chile.
Size Observed attacked Observed not attacked Total
Large 8 28 36
Medium 13 23 36
Small 20 16 36
Total 41 67 108
Small models were attacked significantly more often than medium and large models
(loglinear partial χ2 = 7.86, df = 1, p = 0.005).

Table 2.
Clay models, by habitat, attacked by birds during mid-March of 2012 at El Colorado, Chile.
Habitat Observed attacked Observed not attacked Total
Rock 14 22 36
Ground 21 15 36
Bush 6 30 36
Total 41 67 108

Models in protected habitat under bushes were attacked significantly less often than those
in the open habitat on rock or ground (loglinear partial χ2 = 12.05, df = 1, p = 0.001).
most suspected species, shrike-tyrants and miners (Agriornis and Geositta
spp., respectively) at the study site. We did not capture any images of those
species attacking models, but 12 pictures showed Geositta sp. in close proximity
to the models.

After radiotracking females for almost four months, we discovered that
pregnant females mostly remained with their social group, but in late-term
frequently took solitary refuge beneath large, flat rocks in brushy microhabitats
situated 10–50 m from the open rock outcrops. This behaviour contrasts
with that observed for non-pregnant adult and juvenile females (and males)
who, in the course of two field seasons, were rarely seen in brushy microhabitats
(Santoyo-Brito, 2017). Most importantly, we discovered that females
gave birth in solitary underneath such rocks (i.e., natal chambers) largely
covered by dense low vegetation (Berberis sp.). Radiotracking information
indicated that mothers stayed inside the natal chambers with their 3–4 newborns
for at least 24 h after parturition.
While observing a pregnant female underneath a flat rock through the
borescope, we recorded an agonistic behaviour, the female bit the tip of the
12 Behaviour (2021) DOI:10.1163/1568539X-bja10065
borescope at least six times. We had never observed this agonistic behaviour
in any other context (including 150–200 borescope observations of adults in
solitary and group refuges). To our surprise, the female was giving birth to
three neonates at that exact moment in this natal chamber. It was possible
to observe the newborns still moving inside their clear, compacted, marblelike
embryonic sacs, and the immediate substrate in contact with the embryo
was visibly moist. This was the first scientific record of a L. leopardinus
mother giving birth in the field. We do not know if mothers help the neonates
escape from their tight embryonic sacs. However, in the video, it is possible
to see the mother biting at what seems to be an embryo still in its embryonic
sac (see Video 1 at 10.6084/m9.figshare.13522652). In separate, laboratory
situations, we sometimes had to help neonate L. leopardinus escape from
their embryonic sacs or they died.

We discovered a total of three natal chambers and placed a motionsensitive
camera pointing to the entrance of all three chambers to document
any parental behaviour by the mother and the behaviour of neonates.
Radiotracking information, borescope observations, and video-recordings
suggested that during the first 24 h, mothers and neonates did not leave
the natal chamber. Some 20 h post-parturition, we video-recorded a recent
mother, who was located facing outward partially in an entrance of the natal
chamber. With all four limbs in contact with the ground, she vigorously
moved both front and hind legs to move surrounding soil into the entrance,
piling up soil at the entrance (see Video 2 at 10.6084/m9.figshare.13522652).
Interestingly, on three different instances we observed packed soil heaped up
against the entrance of other natal chambers. Although we did not videorecord
the females moving the soil and pebbles to close the entrance in
these other cases, the marks on the substrate suggested this behaviour. Our
observations indicated that mothers closed the entrances to the natal chamber
with soil when they left, sealing the neonates inside, possibly to prevent
the young, susceptible neonates from prematurely leaving the protection of
the natal chamber. We confirmed the presence of the neonates inside sealed
chambers 24 h after parturition via borescope observations. Video-recordings
and borescope observations indicated that neonates continued to occupy the
chambers without their mother inside for 2–5 days. During the first 2–3 days
after parturition, the mothers were radio-located and observed basking at the
entrance or nearby their natal chambers and nearby their neonates when they
emerged, possibly to protect them. Before and after parturition the mothers
E. Santoyo-Brito et al. / Behaviour (2021) 13

Figure 2. Percent sightings less than 5 m from the mother’s natal chamber for (A) prepartum
mothers (46 sightings), (B) parturient mothers for birth day plus 5 days after (13 sightings)
and (C) postpartum mothers greater than 5 days after giving birth (18 sightings) at El Colorado,
Chile, during austral summer 2013.
were located more often on the rock outcrops distant from their natal chambers
(Figure 2). This change in behaviour was significantly different among
prepartum, parturient, and postpartum mothers when combined sightings of
mothers were analyzed by a Chi-squared test of heterogeneity (χ2 = 20.47,
df = 2, p <0.001). All three individual mothers showed the same significant
pattern. In only 29 of the 1000 iterations did all three mothers show the same
pattern of proximity to the natal chamber as in Figure 2 when all distances
from the natal chamber of each mother were randomly scrambled across the
three time periods, while retaining the same sample size per mother per time
period (randomization test, p <0.05).
After the capture and subsequent radiotracking of two neonates in late
summer (and visual resightings of a third one without a radio), we observed
that neonate L. leopardinus are solitary and very secretive. They can be
found — rarely — in the open, but mostly they remain concealed under flat
rocks covered by dense bushes (Berberis sp.). Neonates were radiotracked
for a total of 40 lizard-days, and were found mainly underneath flat rocks
similar to their natal chambers. Only occasionally did they move into a bush.
Up to the end of our field season in late April, neonates spent a couple
of days in a torpid state under a flat rock, and then moved to another flat
rock usually <1–2 m distant and remained under that rock for a day or two
14 Behaviour (2021) DOI:10.1163/1568539X-bja10065
Figure 3. Percent sightings in which distance moved between consecutive sightings was less
than 5 m, comparing (A) neonates (open bar) with pooled adults and older juveniles (shaded
bar) during the same time of the year, March and April, 2013 and (B) young yearlings (open
bar) with pooled adults and older juveniles (shaded bar) during the same time of the year,
November and December, 2013, both at El Colorado, Chile.
even on clear and sunny days. The randomization test indicated that neonates
(N = 3, mean distance between consecutive points = 3.5 m, SD = 3.0 m)
traveled much shorter distances than adults and juveniles (N = 26, mean
distance between consecutive points = 25.7 m, SD = 26.7 m) during the
same time of the year (March-April): in only 13 cases out of 1000 random
draws of the mean distances between consecutive locations of adults and
juveniles pooled was the mean as small or smaller than the mean distance
travelled by neonates (p = 0.013). Figure 3A shows the basis of this significant
difference in movement of neonates vs. adults and older juveniles when
consecutive distances moved less than 5 m are plotted. With respect to habitat
use, neonates were never found on rock outcrops, whereas pooled adults
and juveniles from the same time period mostly were (χ2 = 146.51, df = 1,
p <0.001).
It seems feasible that the neonates overwinter solitarily underneath large
flat rocks in brushy habitat. Temperatures underneath such rocks with microhabitat
similar to that used by neonates offered thermoregulatory advantages,
especially at night. The mean maximal overnight temperature (8:00 pm to
6:00 am) underneath flat rocks (mean = 12.5°C; SD = 1.14) was warmer
than that under a nearby bush (mean = 9.5°C; SD = 1.11; paired t -test,
t = 5.87, df = 7, p = 0.001). Mean maximal daytime temperatures under
E. Santoyo-Brito et al. / Behaviour (2021) 15
the rock and bush were not significantly different (paired t -test, t =−1.198,
df = 7, p = 0.27). The Kolmogorov–Smirnov test indicated that the distributions
of paired differences between mean maximal temperature under flat
rocks and under nearby bushes for both the day and night intervals were not
different from the normal distribution (p = 0.998 and 0.972, respectively).
Neonates were not found in larger social groups until the next active season
when they became yearlings. In November (early austral spring) of 2013,
we captured four and radio-tagged and followed three young yearling lizards
and radiotracked them for a total of 31 lizard-days. These were bigger (mean
SVL = 48.75 mm) and more agile than the neonates from the fall before
(mean SVL = 40.6 mm), and located in transitional habitat. Mostly they
hid under dense Berberis bushes growing at the base of the large rock outcrops,
sometimes for several days at a time. Young yearlings were sometimes
found solitary and sometimes with older conspecific juveniles and adults at
or near the large rock outcrops. When located under bushes, young yearlings
remained immobile and were very hard to spot. They occasionally made brief
forays up onto the outcrops or back to their vegetated natal habitat. One
young yearling was found in a small crevice where it stayed overnight with
three adults: two males and one female. All four lizards emerged healthy
and unharmed the next morning. These young yearlings, like the neonates
of the fall before, moved very little compared to adults and juveniles at the
same time of the year. The randomization test indicated that young yearlings
(N = 3, mean distance between consecutive locations = 6.42 m, SD =
2.75 m) traveled significantly shorter distances than adults and juveniles
(N = 16, mean distance between consecutive locations = 24.81 m, SD =
17.59 m) during November-December: in only 6 cases out of 1000 random
draws of the mean distances between consecutive locations of adults and
juveniles pooled was the mean as small or smaller than the mean distance
traveled by young yearlings (p = 0.006). Figure 3B shows the basis of this
significant difference in movement of young yearlings vs. adults and older
juveniles when consecutive distances moved less than 5 m are plotted. With
respect to habitat use, young yearlings were found in brushy habitat away
from the rock outcrops significantly more frequently compared to adults and
juveniles, who were mostly found on the open outcrops (χ2 = 30.64, df =
1, p <0.001).
16 Behaviour (2021) DOI:10.1163/1568539X-bja10065
4. Discussion
We hypothesized that avian predation would be stronger on models representing
the neonate size class than on older juvenile and adult size classes,
and predation would be weaker on models under cover than in the open.
Our results support those hypotheses. During March-April, when females
give birth, birds are abundant at our study site and it was very common
to see foraging Geositta and Agriornis spp., known predators of neonate L.
leopardinus (Ridgely & Tudor, 1994; Santoyo-Brito et al., 2014). Neonatesized
models, simulating newborn L. leopardinus, were more often attacked
by avian predators than larger models. Other studies have shown that small
individuals in relation to conspecific adult-sized ones tend to suffer greater
predation (Janzen, 1993; Rivas et al., 1998; Kacoliris et al., 2013).
While it is true that a larger prey provides a bigger meal for the predator
and therefore a greater nutritive benefit (optimal foraging theory), consumption
of very large items requires longer handling, sustains processing costs,
and increases risk of injury (Cooper & Stankowich, 2010). In fact, there
is often a prey-size threshold above which specific prey are undesirable to
predators because they are harder to capture, handle, and consume (Krebs &
Davies, 1993; Scharf et al., 2000; Hawlena & Pérez-Mellado, 2009). Adult
male and female L. leopardinus are fairly large (mean SVL = 100.8 and
99.6 mm, respectively) compared to neonates, young yearlings, and older
juveniles (mean SVL = 40.6, 48.75, and 60.2 mm, respectively). Because
birds do not chew and can only minimally reduce the size of their prey
before ingestion by removal of wings, legs, etc., it is probable that due to
gape-limitation, birds more often attacked neonate-sized models. In a similar
example, the Izu Islands Thrush (Turdus celaenops), a gape-limited
insectivorous bird, consumes only smaller juveniles of the abundant lizard,
Plestiodon latiscutatus (Hasegawa, 1990; Brandley et al., 2014). It is possible
that gape-limitation forces the South American Rufous-banded Miner
(G. rufipennis) and the Black-billed Shrike-tyrant (A. montana) to consume
mostly L. leopardinus neonates and not juveniles and adults. This could be
particularly true for G. rufipennis, since it was previously known only as a
ground-gleaning omnivore and until recently there was no record of predation
on animals other than invertebrates (Santoyo-Brito et al., 2014).
Not surprisingly, models of L. leopardinus located on open rock or soil
were more often attacked by birds than models under vegetative cover.
A similar predation pattern has been described using models of hatchling
E. Santoyo-Brito et al. / Behaviour (2021) 17
broad-headed snakes (Hoplocephalus bungaroides). Exposed models were
attacked by birds significantly more than those under rocks (Webb & Whiting,
2005). It is likely that neonate L. leopardinus move little and mostly
remain hidden under flat rocks in the habitat of the natal chambers through
the fall because of the heavy avian predation pressure at this time. They tend
to take refuge in places surrounded by dense bushes with long, sharp spines,
making it nearly impossible to capture them. A similar behaviour has been
reported in the green iguana (Henderson, 1974). Predation has been considered
an important ecological pressure that determines habitat use of various
lizard species in Chile (Jaksic & Simonetti, 1987). Neonate L. leopardinus
show only minor differences in colour pattern when compared to juveniles
or adults. Thus, we discard the hypothesis that the colouration of neonates
makes them more visually attractive to predators (Martín & López, 1999;
Stuart-Fox et al., 2003).
In oviparous species, oviposition-site selection is a non-random behavioural
choice. In many instances the site selected by the mother may offer
both direct and indirect benefits (e.g., reduced egg detection by predators,
egg development in a suitable microclimate, and habitat safe from predators
after hatching). All those benefits increase her fitness (Smiseth et al.,
2012; Huang et al., 2013). Obviously, in viviparous species, the mother
even more directly protects the developing embryos. It would seem that
viviparity might generally evolve because of this increase in fitness from
the mother’s better protection, given that the cost to the mother is not prohibitive
(Pincheira-Donoso, 2012). In fact, viviparity has evolved repeatedly
from oviparity at least 100 times independently across squamate reptiles,
notably in lizards (Shine, 2005; Blackburn, 2015). Liolaemus leopardinus
is viviparous, so apparently fitness advantages of viviparity prevailed in its
ancestors and probably still today are apparent in this species. But how do
pregnant L. leopardinus females maximize the fitness of their young once
they are born? We documented that mothers leave their social groups on open
bare rock habitat in search of suitable natal chambers located in protected,
brushy habitat (where neonate-sized models were less prone to predation
by birds) to give birth to frail newborns who are not as agile and are less
coordinated than older conspecifics (ESB, SPF, SFF, personal observations).
The poor motor skills of the neonates contrast with the highly altricial recent
newborns of sympatric lizard species L. bellii and L. nigroviridis, which can
be seen running and hiding in the same brushy habitat. Mothers in many
18 Behaviour (2021) DOI:10.1163/1568539X-bja10065
ungulate species show changes in habitat preference during parturition and
early lactation, sometimes choosing brushier, more concealing vegetation
(Gosling, 1969; Jarman, 1976; Leuthold, 1977; Bongi et al., 2008; Ciuti et
al., 2009; Roberts & Rubenstein, 2014). Mothers of L. leopardinus stay with
their neonates in the natal chamber for at least the first 24 h after parturition.
The mothers were radio-located and observed basking at the entrance
or nearby their natal chambers and emerged neonates some 2–3 days after
parturition, probably guarding them or the nest, an example of postpartum
parental care. Although most reptiles are highly precocial to independent
upon birth or hatching (Davis et al., 2013), postpartum parental care has been
documented in at least 60 oviparous and viviparous lizard species from more
than 10 families including Liolaemidae (Somma, 2003a; Halloy et al., 2007;
While et al., 2014). We did not quantify the benefit to neonates from the
maternal behaviour. However, it has been shown that even relatively simple
forms of mother-offspring associations during early postnatal periods benefit
the newborns by improving their antipredation behaviour, levels of activity,
boldness, and exploration (Munch et al., 2018).
Borescope videos of very young newborn L. leopardinus in their natural
natal chambers in the field and our manipulations with captive-born others
revealed that neonates were frail and very vulnerable to harm. Field observations
and video-recordings showed that when the mother left her natal
chamber, she packed the entrances with soil, possibly to prevent neonates
from leaving the chamber, and, thus, indirectly protecting them from predation.
Video-recordings and radio-tracking data indicated that mothers were
observed and located on several occasions close to the natal chambers, their
neonates, and away from their social groups on bare rock outcrops. A similar
behaviour has been reported in pregnant Liolaemus elongatus, another
viviparous, high-elevation Andean lizard (Halloy et al., 2007).
The repetitive aggressive behaviour shown by one mother as she was giving
birth in the field (gaping at, charging, and biting the tip of the borescope)
might be a case of direct parental care, especially since this aggressiveness
contrasts with the otherwise non-aggressive behaviour that characterizes this
species (Fox & Shipman, 2003; Santoyo-Brito, 2017; Santoyo-Brito et al.,
2017). It is possible that mothers show agonistic behaviour only during the
time when the neonates are still inside their embryonic sacs, when their
newborns are possibly the most vulnerable to predation. Likewise, staying
with the neonates for a time inside the natal chambers and then later nearby
E. Santoyo-Brito et al. / Behaviour (2021) 19
the chambers when the neonates venture outside a bit might be protective
parental care by the mother. Other squamate species show aggression against
predators and protective behaviour when their offspring are present (Greene
et al., 2002; Sinn et al., 2008; Huang et al., 2013; Sherbrooke, 2017), and we
have observed adult L. leopardinus showing protective guarding behaviour
against us in the field (but not biting) when they were with older juveniles.
We suggest that L. leopardinus may show parental care especially of
neonates but even of older, free-ranging juveniles.
None of the radiotracked newborns were observed or located in proximity
to conspecifics after they left the area outside the natal chamber. Neonates
moved very short distances over the day, significantly less than adults and
juveniles. They were located mainly underneath flat rocks similar to the natal
chambers, and only occasionally moved to ground cover, but were never
located on the rock outcrops inhabited by adults and juveniles. We suggest
that the neonates’ secretive behaviour is a strategy to decrease their vulnerability
to predation by birds. After overwintering underneath flat rocks, the
neonates emerged as bigger and more agile yearlings. They continued to
behave very cryptically and moved around significantly less than adults or
older juveniles at the same time of the year. Gradually these young yearlings
moved toward the rock outcrops, but mostly stayed in bushes. Significantly
fewer sightings of them were made on the open, rock outcrops compared to
adults and older juveniles.
In a striking sense, L. leopardinus neonates behaviourally resemble one
category of newborn ungulates, but in an extended temporal way. Relative to
adults, ungulate infants are particularly vulnerable to predation due to their
smaller size and poorer escape ability (Leuthold, 1977; Bleich, 1999; Barber-
Meyer & Mech, 2008). Consequently, young bovids, cervids and equids
adapt one adaptive anti-predator strategy or another; they can be divided
into ‘follower’ and ‘hider’ species, depending upon their infant behaviour
(Walther, 1965, 1969; Lent, 1974; Leuthold, 1977). Very young infants of
‘hider’ species spend more time in hiding in solitary away from their mother
and other conspecifics, and then gradually transition to less hiding and more
activity until they join the social herd (Costelloe & Rubenstein, 2015). Older
transitional fawns are more susceptible to predation even though they are
older and more agile because they are more detectable due to their change in
behaviour (Fitzgibbon, 1990; Byers, 1997; Costelloe & Rubenstein, 2015).
The young of ‘follower’ species stay with the mother and the social group
20 Behaviour (2021) DOI:10.1163/1568539X-bja10065
from birth on and rely on the group for protection from predators (Hamilton,
1971; Leuthold, 1977; King et al., 2012; Costelloe & Rubenstein, 2015). So
neonate L. leopardinus are like ‘hiding’ species of ungulates, except that the
mother does not return to the hidden neonate for nursing or other maternal
care. Neonate L. leopardinus remain in their hiding phase to and through
brumation (longer than in ungulates) and only the following spring begin to
make the transition toward social life with the adults and older juveniles on
the rock outcrops. Perhaps it is not wise to extend the comparison of lizards
and ungulates too far, but there are other species of viviparous social lizards
in which the neonates stay with the social groups from birth on, much like
the ‘follower’ species of ungulates. Examples are Xantusia vigilis (Davis et
al., 2011), Egernia stokesii (Duffield & Bull, 2002; Lanham & Bull, 2004;
Gardner et al., 2016), E. whitii (Chapple & Keogh, 2006), and E. striollata
(Duckett et al., 2012). We are unaware, however, if there are other examples
of ‘hider’ social species of lizards, like L. leopardinus.
Female parturition occurs when nighttime temperatures grow colder,
about two months before brumation. Nighttime temperatures were significantly
warmer under flat rocks similar to natal chambers than inside bushes
during this time. We suggest that the thermoregulatory advantage is an indirect
benefit to the neonates from their mothers’ nest-site selection in addition
to the benefit of decreased risk of predation in the more vegetated habitat
away from the open, rock outcrops. Neonates extend this advantage by
selecting the same habitat until they enter brumation.
We discard the possibility of competition molding the described behaviour
of L. leopardinus mothers and neonates. Liolaemus leopardinus is not agonistic
toward conspecifics for access to resources. The species is passive and
rarely fights or displays (Fox & Shipman, 2003). It likely uses chemical signaling
in place of escalated visual communication (Fox & Shipman, 2003).
Extensive home range overlap within and between sexes and the grouping
behaviour during day and night clearly shows that lizards do not defend or
compete for territories (Fox & Shipman, 2003; Santoyo-Brito, 2017). We
have never observed any cannibalistic or aggressive behaviour by adults
against neonates or young individuals in the field or laboratory (Santoyo-
Brito et al., 2017). Although we did not measure food availability, apparently
it was not a limiting resource during the period of our study; invertebrates
and plant matter were abundant during the lizard active season, and we never
observed intraspecific competition over food (Santoyo-Brito, 2017).
E. Santoyo-Brito et al. / Behaviour (2021) 21
Our study calls for more extensive comparative research across populations
of L. leopardinus experiencing different levels of avian predation pressure
to more definitively determine that it is avian predation that is responsible
for the parental behaviour of L. leopardinus mothers and the secretive,
solitary behaviour of the neonates. It has been well established that both
ecological and climatic (i.e., high predation pressure and harsh environmental
conditions) can promote the expression of parental care (Clutton-Brock,
1991; Huang & Wang, 2008; Smiseth et al., 2012; Pike et al., 2015). This is
true especially in species that inhabit cold-temperate environments, exhibit
high reproductive effort (Halloy et al., 2007; Huang et al., 2013; Cabezas-
Cartes et al., 2018), and have a limited supply of energy for reproduction.
All these are characteristics of the high-elevation and highly social L. leopardinus.
We hope our findings might stimulate other studies of neonate and
maternal behaviour and avian predation pressure at high elevations in other
species in other places.
Acknowledgements
We thank J. Grindstaff, M. Lovern and T. O’Connell for critically reading the
manuscript and offering constructive input throughout the study. We thank
field assistants D. Esquerré, M. Palma, N. Torres Achiles and J. Masseloux.
Permission to conduct this research was given by Oklahoma State University
IACUC according to ACUP AS-11-13, and by Servicio Agrícola Ganadero,
Chile permit Nos 188 and 303. Conflict of Interests: The Authors declare
that they have no conflict of interests. This study was funded by The National
Geographic Society, Delta Foundation, the Southwestern Association of Naturalists,
and Oklahoma State University.
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Table A1.
Tracking information (pooled radiolocations and visual sightings) of neonates and pooled
adults and older juveniles in March and April, 2013, and of young yearlings and pooled
adults and juveniles in November and December, 2013, at El Colorado, Chile.
Age and season Individual Age1 Sex2 Day observed Total
sightings
First Last
Neonates in March
and April
GOOG N – 28-Mar-13 25-Apr-13 9
OOYY N 2 16-Apr-13 26-Apr-13 9
OYOO N 1 19-Apr-13 27-Apr-13 2
Total 20
Adults and older
juveniles in
March and
April
BBBW J 1 12-Mar-13 26-Mar-13 3
BBRB A 2 4-Apr-13 4-Apr-13 13
BGBG A 2 8-Mar-13 13-Apr-13 7
BWBW A 2 2-Mar-13 11-Apr-13 21
GGOG A 1 26-Mar-13 16-Apr-13 3
GGOO A 1 5-Mar-13 12-Apr-13 2
GOGO J 2 12-Apr-13 17-Apr-13 2
GOOO J 1 12-Apr-13 20-Apr-13 2
GRRG A 1 21-Mar-13 23-Mar-13 2
GWWW A 1 16-Mar-13 27-Mar-13 2
OGGO A 1 6-Mar-13 8-Apr-13 2
OOGG A 1 2-Mar-13 13-Apr-13 4
OWWW J 1 5-Mar-13 27-Mar-13 2
OYYO A 1 17-Apr-13 18-Apr-13 2
RBBB J 2 26-Mar-13 6-Apr-13 2
RRYR A 1 12-Mar-13 24-Mar-13 2
WBBB A 2 24-Mar-13 29-Mar-13 2
WOOO A 1 16-Mar-13 8-Apr-13 3
WOWO A 2 14-Mar-13 12-Apr-13 11
E. Santoyo-Brito et al. / Behaviour (2021) 29
Table A1.
(Continued.)
Age and season Individual Age1 Sex2 Day observed Total
sightings
First Last
Adults and older
juveniles in
March and
April
(Continued)
WOWW A 2 1-Mar-13 15-Mar-13 8
WRWR A 1 29-Mar-13 13-Apr-13 2
WWWG A 1 5-Mar-13 8-Apr-13 2
YWWW J 1 5-Mar-13 8-Mar-13 2
YWWY A 2 1-Mar-13 16-Mar-13 10
YYYW A 2 1-Mar-13 9-Apr-13 13
Total 124
Young yearlings in
November and
December
OORR Yy 1 12-Nov-13 01-Dec-13 11
ORRO Yy 2 17-Nov-13 18-Nov-13 2
ROOR Yy 2 12-Nov-13 18-Nov-13 5
Total 18
Adults and older
juveniles in
November and
December
BBBW A 1 08-Nov-13 01-Dec-13 13
BWWB J 2 15-Nov-13 21-Nov-13 2
GRRR A 1 20-Nov-13 01-Dec-13 5
GWGW A 2 08-Nov-13 09-Nov-13 2
RBRB A 2 14-Nov-13 01-Dec-13 11
RROO A 2 15-Nov-13 30-Nov-13 3
WWYY A 1 08-Nov-13 01-Dec-13 9
Total 45
1Age: N, neonate; Yy, 7–8-month-old juvenile; J, older juvenile; A, adult.
2Sex: 1, Male; 2, Female.