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ORIGINAL PAPER
Does social environment influence learning ability in a family-
living lizard?
Julia L. Riley
1
•Daniel W. A. Noble
2
•Richard W. Byrne
3
•Martin J. Whiting
1
Received: 13 July 2016 / Revised: 8 December 2016 / Accepted: 19 December 2016
ÓSpringer-Verlag Berlin Heidelberg 2016
Abstract Early developmental environment can have
profound effects on individual physiology, behaviour, and
learning. In birds and mammals, social isolation during
development is known to negatively affect learning ability;
yet in other taxa, like reptiles, the effect of social isolation
during development on learning ability is unknown. We
investigated how social environment affects learning abil-
ity in the family-living tree skink (Egernia striolata). We
hypothesized that early social environment shapes cogni-
tive development in skinks and predicted that skinks raised
in social isolation would have reduced learning ability
compared to skinks raised socially. Offspring were sepa-
rated at birth into two rearing treatments: (1) raised alone
or (2) in a pair. After 1 year, we quantified spatial learning
ability of skinks in these rearing treatments (N=14 soli-
tary, 14 social). We found no effect of rearing treatment on
learning ability. The number of skinks to successfully learn
the task, the number of trials taken to learn the task, the
latency to perform the task, and the number of errors in
each trial did not differ between isolated and socially
reared skinks. Our results were unexpected, yet the
facultative nature of this species’ social system may result
in a reduced effect of social isolation on behaviour when
compared to species with obligate sociality. Overall, our
findings do not provide evidence that social environment
affects development of spatial learning ability in this
family-living lizard.
Keywords Squamate Sociality Cognition Ontogeny
Facultative sociality
Introduction
Animals learn by acquiring, processing, storing, and then
acting on information collected from their environment
(Dukas 2009; Shettleworth 2010; Buchanan et al. 2013).
An individual’s ability to learn can be adaptive by influ-
encing behaviours with ecological significance, like for-
aging, competition, mating, anti-predatory behaviour, and
dispersal (Dukas 2009; Buchanan et al. 2013). For exam-
ple, American bird grasshoppers (Schistocerca americana)
that readily learnt a foraging task exhibited a 20% higher
growth rate than non-learners (Dukas and Bernays 2000);
great tit (Parus major) parents that learnt a novel task had
higher offspring survival and more offspring (Cauchard
et al. 2013); and male satin bowerbird (Ptilonorhynchus
violaceus) problem-solving performance relates positively
to their mating success (Keagy et al. 2009; but see Isden
et al. 2013 for contrasting results with spotted bowerbirds,
Chlamydera maculata). These studies provide evidence of
a link between animal learning and fitness (but see Thorton
et al. 2014 for methodological concerns). Although learn-
ing is a crucial trait for the survival and reproduction of
some species, there are many factors that affect learning
ability. Environmental severity (Shettleworth 2010,
Electronic supplementary material The online version of this
article (doi:10.1007/s10071-016-1068-0) contains supplementary
material, which is available to authorized users.
&Julia L. Riley
julia.riley87@gmail.com
1
Department of Biological Sciences, Macquarie University,
Sydney, NSW, Australia
2
School of Biological, Earth, and Environmental Sciences,
University of New South Wales, Kensington, NSW, Australia
3
School of Psychology and Neuroscience, University of St.
Andrews, St. Andrews, Fife, UK
123
Anim Cogn
DOI 10.1007/s10071-016-1068-0
pp 371–394; Roth et al. 2010), rapid environmental change
as experienced during urbanization (Sih et al. 2011; Sol
et al. 2013), experimental methods (Noble et al. 2012), and
sociality (Zuberbu
¨hler and Byrne 2006; Burkart and van
Schaik 2009) are known to affect learning ability. In
addition, individual-specific traits such as sex (Carazo et al.
2014), personality (Sih and Del Giudice 2012; Carazo et al.
2014), age (Noble et al. 2014), as well as early develop-
mental environment (Stamps and Groothuis 2010; Clark
et al. 2013) are linked to learning ability.
The social environment during early development can
influence an individual’s learning ability throughout their
lifetime (Cacioppo and Hawkley 2009). This relationship
between social environment and learning ability was first
demonstrated in the 1960s through Harlow’s research on
rhesus macaques (Macaca mulatta). Rhesus macaques live
in large, mixed-sex groups (*10 individuals; Melnick
et al. 1984), and females care for their young from birth
until the birth of their next offspring (Fooden 2000). Har-
low’s research isolated juvenile rhesus macaques from any
social interaction; development in social isolation debili-
tated these individuals in many ways, including signifi-
cantly impairing learning ability (Harlow et al. 1965).
Subsequently, numerous studies have also demonstrated a
negative relationship between social isolation and learning
in rats (Rattus norvegicus; Greenough et al. 1972; Morgan
et al. 1975; Einon 1980; Juraska et al. 1984; Holson 1986),
although a few studies examining rats and chickens (Gallus
gallus domesticus) have found variable and/or positive
effects of isolation on learning (Wongwitdecha and Mars-
den 1996; Frisone et al. 2002; Goerlich et al. 2012).
Overall, it is well established that social environment, or
lack thereof, can affect learning ability in mammals and
birds. So far, studies have been taxonomically biased
towards endotherms (e.g. birds and mammals) with obli-
gate social systems. There has been little research on how
social isolation affects learning in ectotherms (e.g. fish and
reptiles).
There is increasing evidence that reptiles exhibit diverse
social systems that can be kin-based (Doody et al. 2012;
Gardner et al. 2015). For example, Australian skinks in the
Egernia group exist in stable social aggregations, some
with kin, some exhibiting long-term monogamy, and even
parental care of offspring (Chapple 2003; Gardner et al.
2015; While et al. 2015). Egernia striolata (the Australian
tree skink) is known to aggregate in social groups con-
sisting of mating adult pairs, parents with offspring, and
juveniles (Bonnett 1999; Duckett et al. 2012). Yet, inter-
estingly, the social structure of E. striolata is highly vari-
able both within and between populations. Within
populations, skinks can be either found alone or in groups
of variable size (2–10 skinks; Bustard 1970; Bonnett 1999).
Across the tree skink’s range, different social systems have
been described between populations. In arboreal popula-
tions, tree skinks have been found in small groups (maxi-
mum of three individuals) and most often found alone
(Bustard 1970; Cunningham et al. 2007). Yet, in other
arboreal and in saxicolous populations, tree skinks were
most often in larger social groups (\10 lizards) of closely
related individuals (Swanson 1976; Ehmann 1992, p. 242;
Bonnett 1999; Michael and Cunningham 2010; Duckett
et al. 2012). In the wild, groups consisting of parents and
offspring are the most common, yet groups of only juve-
niles do exist (Bonnett 1999; Duckett et al. 2012, Riley
unpubl. data). These juvenile-only groups vary in size,
ranging from pairs to four individuals; often juveniles are
also observed on their own (Bonnett 1999; Michael and
Cunningham 2010; Duckett et al. 2012). This social nature
of E. striolata makes it a good model for studying the
influence of social environment on learning ability. We
examined the effect of development in social isolation
versus within a social group, and hypothesized that
development in social isolation would affect the learning
ability of E. striolata. As the Egernia group of skinks
exhibit similar social behaviours to birds and mammals, we
expected that social environment would similarly affect
development of reptile behaviour. Thus, we predicted that
(1) fewer skinks raised in social isolation would learn a
spatial maze task, and (2) it would take longer for skinks
raised in isolation to learn the task compared to skinks
raised socially.
Methods
Study species, collection, and husbandry
Tree skinks are a viviparous skink found across south-
eastern Australia. They inhabit hollow limbs of, and cracks
under the bark of, standing trees or within fallen timber, as
well as crevices on rock outcrops (Cogger 2014, p. 549).
We collected 15 gravid female E. striolata from near
Albury, New South Wales (-35.980S, 146.970E), and held
them at Macquarie University until parturition. Parturition
occurred from 10 February to 12 March 2014. Offspring
were separated from females and randomly allocated into
two treatments, social and isolated, on 14 April 2014 (after
baseline behavioural trait assays occurred; Riley unpub-
lished data). The social treatment consisted of two unre-
lated juveniles housed together (N=14 lizards within
seven pairs; four males and ten females); in the isolated
treatment, lizards were housed alone (N=14 lizards; eight
males and six females). Juvenile social groupings of similar
sizes have been reported for wild populations of E. strio-
lata (Chapple 2003), although social groups most often
consist of parent(s) and offspring (Chapple 2003).
Anim Cogn
123
Including parents in our social treatment was logistically
not feasible because adult Egernia, particularly females,
are known to be highly aggressive towards juveniles
(O’Connor and Shine 2004; Sinn et al. 2008). In fact,
infanticide is common in multiple Egernia group spp.
(Lanham and Bull 2000;Post2000; O’Connor and Shine
2004), and there are even instances wherein females eat
their own offspring (E. stokesii, Lanham and Bull 2000;E.
striolata, Riley pers. obs. 2015). We housed juveniles
within their rearing treatments for approximately 1 year
before we conducted our learning assay (17 May to 4 June
2015).
Learning assay
We quantified the learning ability of juvenile E. striolata
(N=28) with a spatial learning task. During the assay, we
housed juveniles in a paper-lined rectangular arena (base
dimensions 390 mm W 9580 mm L 9455 mm H) con-
taining a water dish and a refuge (120 mm W 9
175 mm L 938 mm H). A 100-W heat lamp directed at
the refuge, which allowed lizards to thermoregulate, lighted
each arena. We did not feed lizards during the assay; the
only food they received was the food reward (1.25 ml of
pure
´ed fruit; Heinz
Ò
apple and mango, apple, and pear)
offered twice daily, and eaten only if the trial was completed
successfully. Prior to trials commencing, we gave lizards
24 h to acclimate to their novel housing area.
We tested spatial learning ability using a vertical maze.
This is a biologically relevant task, because in the wild E.
striolata forage within their rock and tree habitats by ver-
tically climbing from one crevice to another (Riley pers.
obs. 2015). In our spatial learning task, the lizards had to
navigate a set of five ladders and three ledges to access a
food reward (see Supplementary Video 1). In stage one of
the task, lizards had to choose between one of three mesh
ladders running from the ground to one of two wooden
ledges (Fig. 1). If done correctly, in stage two, lizards then
had a choice between one of two ladders running from
these wooden ledges to a third ledge that held the food
reward (Fig. 1). Incorrect ladders at all stages were par-
tially covered with clear tape, so the lizard could not
completely climb them but they looked identical to the
correct ladder. The slippery, clear tape covered the mesh
ladders starting at 50 mm above the ground (50 mm is
approximately half the body length of our skinks; Fig. 1).
So, unless the lizard attempted the climb the ladder, it
could not feel or see a difference between the ladders at
ground level. We randomized the position of the correct
first ladder to control for lateralization bias (Fig. 1). In
other words, either the first left-most ladder or the second
right ladder was climbable, or vice versa. We randomly
assigned an equal number of lizards to each set-up. This
task was attached to a laminated plywood board
(390 9305 mm), and during trials, it was placed along the
side of the trial tub opposite to the refuge (Fig. 1). The task
had both intra-maze spatial cues (e.g. black circle on right
and diagonal stripes on left) and extra-maze spatial cues
(e.g. the location of items outside the trial bin) that the
lizards could have used to navigate the task (Fig. 1).
At the beginning of each trial, we first removed the water
dish and placed the lizard within its refuge at the opposite
end of the arena to the task (Fig. 1). We would then place
the task-board within the housing bin, and then, marking the
start of the trial, remove the refuge. The trial was remotely
video-recorded using CCTV cameras (model H.264, CCTV
security systems, Melbourne, VIC) for 1 h. We conducted
two trials per day, in the morning (09:00–10:00 h) and the
afternoon (12:00–14:00 h) with a minimum of 2 h between
trials. All lizards were given a maximum of 30 trials to
attempt the task; nevertheless, due to variability in lizard
behaviour, the total number of trials completed varied
between individuals. Most skinks attempted the first stage of
the task for 30 trials, but one skink only interacted with the
first stage of the task for 25 trials. Similarly, most lizards
attempted the full task for 30 trials (N=24), but one skink
interacted with the task for 25 trials, one skink interacted
with the task for 26 trials, and another two skinks interacted
with the task for 28 trials.
From the videos, we scored: (1) successful completion
of task, (2) latency to perform the task successfully, and (3)
number of errors made during each trial. Successful com-
pletion of the task was considered in two stages (Fig. 1).
First, the lizard had to climb the correct first ladder and
reach the ledge. If the lizard attempted to climb (had a
minimum of both forelimbs on a ladder) any of the
incorrect ladders, the task was marked as unsuccessful.
Second, once on the first ledge, the lizards had to move
across the gap between the two ledges, climb the second
correct ladder, gain access to the final ledge, and access the
food reward (see Supplementary Video 1). When lizards
were situated on the first ledge, we observed that they
preferred to grip onto the exposed portion of the incorrect
ladder’s mesh with one, or more, limbs to allow stability,
while they were attempted to move across the ledges. So,
we marked the second stage of the task as successful if the
lizard (1) moved horizontally, or diagonally across the first
ledge and did not encounter the tape-covered portion of the
incorrect ladder, and then (2) climbed the correct second
ladder. If, instead, the lizard moved vertically up the
incorrect ladder and encountered the tape-covered portion,
it was marked as unsuccessful. We separately assessed if
each lizard correctly performed the first stage of the task
(e.g. climbed the correct first ladder; Fig. 1), and the full
task (e.g. climbed both the correct first and second ladders).
We then classified each lizard as a ‘learner’ or a ‘non-
Anim Cogn
123
learner’ by examining the tally of correct/incorrect choices
(Tables S1 and S2). Following Noble et al. (2014), we
considered a lizard to be a ‘learner’ if it successfully per-
formed the task a minimum of 5/6 consecutive times. We
scored latency to perform the task by recording the time
(s) from the start of the trial (as marked by lifting the
refuge from the arena) until the lizard placed its head in the
food dish. We scored latency for the full task only, and for
each trial regardless of whether the task was initially
completed successfully. For example, if a lizard initially
climbed an incorrect ladder but then completed the task, it
would have been unsuccessful at the task, but we would
still measure latency until it accessed the food reward. For
the full task only, we also tallied how many times a lizard
climbed incorrect ladders before it performed the full task
correctly or the trial ended. For all behaviours (task success
for the first stage and full task, latency, number of errors),
there were high levels of congruence in our scoring (see
Supplementary Materials).
Assessment of learning criteria
We assessed robustness of our learning criteria by tal-
lying the number of correct/incorrect choices from the
last trial in the learning criterion to the lizard’s last trial
(e.g. if a lizard performed 5/6 trials correctly, we started
the tally at the 6th trial; Tables S1 and S2). We only
tested the learning criteria for a subset of lizards that had
six or more trials after the trial in which they reached the
criterion. We tested whether this tally of correct/incor-
rect choices was significant according to an exact bino-
mial choice test. For the first stage of the task, 21/23
(91%) of lizards performed the task correctly signifi-
cantly more than expected by chance. For the full
learning task, 16/17 (94%) of the skinks performed the
task correctly significantly more than expected by
chance. These results suggest our learning criterion was
sufficient in categorizing lizards that learnt from those
that did not.
Fig. 1 Schematic diagram of our spatial learning assay arena as set-
up at the beginning of our trials. The clear tape covering the incorrect
mesh ‘ladders’ was not visible, but is included in the diagram for
clarity. The task, the vertical spatial learning maze, was insertable and
was only within the arena during the trial
Anim Cogn
123
Statistical analyses
We analysed our data using generalized linear mixed
effects models (GLMM) with a Bayesian Markov chain
Monte Carlo (MCMC) sampling approach. We used mixed
effect models (GLMMs) to incorporate the dependency
among observations of lizards from the same litter, as well
as repeated observations of the same individual into our
analyses (Dobson and Barnett 2008). MCMC is a simula-
tion technique that we used to obtain the distribution of
each parameter in our GLMMs, and this technique requires
specification of a probability distribution (prior) for the
analysis (Masson 2011; Zurr et al. 2013; Gelman et al.
2014, pp. 3–27; Kruschke 2014, pp. 7–59). We prelimi-
narily ran our GLMMs with multiple priors, but there was
negligible difference between model results with varying
priors. So, we used default diffuse uniform priors for our
fixed effects, and for the random effect variance–covari-
ance matrix our prior specification was V=10
01
and
nu =0.002 (Hadfield 2010). In brief, diffuse priors assign
equal probabilities to all possibilities and typically yield
parameter estimates that are not too different from fre-
quentist statistical analyses (Zurr et al. 2013, pp. 66–72;
Kruschke 2014, pp. 7–59). Analyses were performed in R v
3.0.3 using the MCMCglmm package (Hadfield 2010;R
Core Team 2016).
In each model, we estimated model parameters
2,000,000 times (iterations), discarded the first 10,000
estimations (burn-in), and only sampled the parameter
every 1,000th estimate (thinning interval). We repeated this
procedure three separate times (chains) to reduce the
autocorrelation of successive samples from one chain (Zurr
et al. 2013, pp. 66–72). We verified convergence of chains
using the Gelman–Rubin test in the R package coda
(Plummer et al. 2015). We also visually inspected all plots
of our chains to ensure they were well mixed (i.e. were
sampling randomly). Autocorrelation of the chains for both
fixed and random effects was assessed to ensure levels
were low (lag \0.1) using the autocorr function in R, and
we also performed Geweke and Heidelberg autocorrelation
diagnostics (all from the R package coda; Plummer et al.
2015).
Data from the first stage of the task and the full task
were analysed separately, but the variables included in
each of the models (1–3) were the same (see Table 1for
details):
1. This binomial MCMC-GLMM examined whether the
probability of learning a task (learner =1, non-
learner =0) was influenced by rearing treatment
(isolated or social). We also controlled for sex (fixed
effect) and mother identity (random effect).
2. This Poisson MCMC-GLMM examined whether the
number of trials taken to learn the task was influenced
by rearing treatment, while controlling for lizard sex
and mother identity.
3. This binomial MCMC-GLMM examined whether the
probability of task success during each trial was
influenced by rearing treatment. The model also
included the fixed effects of sex, trial number, and an
interaction between treatment and trial number. It also
included lizard and mother identity as random effects.
4. This Gaussian MCMC-GLMM examined whether
latency to successfully complete the task (transformed
with a square-root transformation to ensure normality
of residuals) was influenced by rearing treatment. The
model also included the fixed effects of sex, trial
number, and an interaction between treatment and trial
number, as well as the random effects of lizard and
mother identity.
5. This Poisson MCMC-GLMM examined whether the
number of errors made during each trial was affected
by rearing treatment. The model also included the fixed
effects of sex, trial number, and an interaction between
treatment and trial number, as well as the random
effects of lizard and mother identity.
We report the mode of the MCMC sample and 95%
credible intervals for our parameter estimates. Parameter
estimates were considered significant when the credible
intervals did not include 0, and the pMCMC values cal-
culated by MCMCglmm were \0.05 (Hadfield 2010).
When we predicted fitted lines from the models for visu-
alization of differences in response variables between
rearing treatments, we set sex, our secondary fixed factor,
to the intercept-level value. Data for this study are avail-
able from https://dx.doi.org/10.6084/m9.figshare.3984111.
v1.
Results
First stage of learning task (three-ladder choice)
Twenty-five of 28 (89%) of the lizards met our learning
criterion for choosing the correct first stage ladder (out of
three possibilities). Whether a lizard learnt or did not learn
the first stage of the task did not depend on rearing treat-
ment (Table 1): 12/14 (86%) socially reared and 13/14
(93%) isolated lizards were categorized as learners. Rear-
ing treatment also did not affect the number of trials taken
to learn stage one of the task. Socially reared skinks took
on average 15 trials (95% CI 10–19) to learn stage one of
the task, and isolated skinks took on average 14 trials (95%
CI 11–17). Males were less likely to learn the first stage of
Anim Cogn
123
Table 1 Pooled posterior modes and 95% credibility intervals from Bayesian Markov chain Monte Carlo generalized linear mixed effect models (MCMC-GLMM) that examined the effect of a
lizard’s social environment (ISOLATED or SOCIAL) on (1) the probability of learning the task, (2) number of trials until learnt the task, (3) probability of task success, (4) latency (s;
transformed using a square-root transformation), and (5) number of errors made during each trial
Probability of learning the task Number of trials until learnt the
task
Probability of task success Latency to access the food
reward
Number of errors
Estimate Lower Upper Estimate Lower Upper Estimate Lower Upper Estimate Lower Upper Estimate Lower Upper
(a) First stage (three-ladder choice)
Intercept 34.70 1.67 331.06 2.53 2.22 2.90 -0.37 -1.24 0.58 – – – – – –
Treatment ISOLATED 5.62 -22.02 183.90 -0.014 -0.47 0.41 0.34 -0.72 1.47 – – – – – –
Sex MALE -31.54 -242.16 -3.03 0.033 -0.43 0.53 -0.90 -1.92 0.40 – – – – – –
Trial number – – – – – – 0.098 0.066 0.13 ––––––
Trial 9treatment – – – – – – 0.01 -0.039 0.055 – – – – – –
(b) The full learning task (three-ladder choice and then a two-ladder choice)
Intercept 1.07 -0.98 9.40 2.74 2.42 3.01 -2.04 -2.91 -0.92 41.64 34.40 47.47 0.44 -0.024 1.05
Treatment ISOLATED 0.66 -2.53 3.75 0.09 -0.27 0.40 -0.66 -1.89 0.71 -1.72 -10.30 6.68 0.37 -0.36 0.92
Sex MALE -1.48 -5.54 2.26 0.014 -0.36 0.42 -0.25 -1.44 0.78 2.21 -3.96 9.24 -0.076 -0.58 0.51
Trial number – – – – – – 0.12 0.090 0.16 -0.38 -0.59 -0.17 -0.071 -0.094 -0.046
Trial 9treatment – – – – – – 0.027 -0.026 0.071 0.097 -0.16 0.44 0.014 -0.013 0.046
Bold values are parameter estimates that were considered significant (i.e. their 95% credibility intervals did not include 0)
These models were used to examine effects for (a) the first stage of the task (three-ladder choice; N
obs
=835, N
lizards
=28), and (b) the full learning task (three-ladder choice and then a two-
ladder choice; N
obs
=827, N
lizards
=28). Models also included additional fixed factors of sex (MALE or FEMALE), trial number, and an interaction between trial and treatment when
appropriate
Anim Cogn
123
the task than females, but there was no sex-effect on the
number of trials taken to learn the task and this observed
sex-effect was not consistent when we examined the full
task (Table 1).
Rearing treatment did not affect probability of task
success during each trial (Table 1; Fig. 2a). There also was
no sex-effect on the probability of task success during each
trial (Table 1). Yet, probability of task success during each
trial increased over time (as trial number increased), which
indicates that, regardless of rearing treatment, tree skinks
were learning stage one of the task (Table 1; Fig. 2a).
Full learning task (three-ladder choice and then
a two-ladder choice)
When we considered the learning task in its entirety (three-
ladder choice followed by a two-ladder choice), 19/28
(68%) of skinks met our learning criterion. Whether a
lizard learnt the full task or not did not depend on rearing
treatment (Table 1): 9/14 (64%) socially reared and 10/14
(71%) isolated lizards were categorized as learners. Rear-
ing treatment did not affect number of trials taken to learn
the full task (Table 1): socially reared skinks took an
average of 16 trials (95% CI 11–21) to learn the task, and
isolated skinks took an average of 17 trials (95% CI
14–19). The probability of learning the full task and the
number of trials taken to learn the task were not signifi-
cantly affected by sex (Table 1).
Similarly, rearing treatment did not affect probability of
task success, latency, or number of errors made during each
trial (Table 1; Fig. 2b). Socially reared skinks took an
average of 1269 s to complete the task (95% CI
1261–1278), and made on average 0.90 incorrect choices
during a trial (95% CI 0.83–0.97). Isolated skinks took on
average 1321 s to complete the task (95% CI 1313–1328)
and made on average 1.26 incorrect choices during a trial
(95% CI 1.20–1.32). There were no sex-effects on proba-
bility of task success during each trial, latency, or number
of errors made during each trial (Table 1). Probability of
task success during each trial increased over time (as trial
number increased; Fig. 2b), and latency to complete the
task (Fig. S1) and number of errors (Fig. S2) during a trial
both decreased over time (Table 1). These results are evi-
dence that tree skinks were learning the full task.
Discussion
Our prediction that social isolation during development
would negatively affect learning ability in E. striolata was
not supported. An almost equal number of skinks in our
two treatments (social vs. isolated rearing environment)
were categorized as ‘learners’ in our spatial learning task.
Moreover, the number of trials it took skinks to learn the
task did not differ between rearing treatments. We found
no effect of rearing treatment on probability of task success
during each trial, latency until task success, and number of
errors made during the trial. All our findings, across anal-
yses for both the first stage of the task and the full task,
consistently demonstrate no evidence for an effect of social
isolation on learning ability of a social skink.
The key to why we found this unexpected result may lie
in the tree skink’s variable social system. As noted above,
the social structure of E. striolata is quite variable; within
one population, individuals can vary from being solitary to
highly aggregative with kin (Bustard 1970; Bonnett 1999;
Duckett et al. 2012). This natural flexibility in group size
and variation in individual sociability may mean that
development in isolation is simply a normal option in the
wild, as such social isolation is possibly less stressful for
this species. Thus, there are limited negative consequences
to this social state. For example, in domestic chickens,
stress (or lack of it) has been suggested as a mechanism
that regulates learning ability (Goerlich et al. 2012). In this
study, isolated chicks actually made more correct choices
in an associative learning task. These chicks had a reduced
stress response, which likely resulted in a higher coping
ability and an enhanced learning ability. It would be
Fig. 2 Predicted probabilities of task success during each trial did not
differ between developmental treatments (social: light grey shading
and dashed line; isolated: dark grey shading and solid line) for either
astage one or bthe full spatial learning task. The darkest shade of grey
is where the 95% predicted credible intervals, which are represented
by shaded polygons around predicted probabilities, overlap
Anim Cogn
123
beneficial to follow up our study on E. striolata by mea-
suring stress levels in both our isolated and socially reared
treatments to examine whether stress may be the mecha-
nism that explains our unexpected findings. All in all, the
plastic social nature of E. striolata may buffer these lizards
from the extreme negative effects of social isolation pre-
viously observed in studies on mammals and birds. These
previous studies often examined the effects of social iso-
lation on species with more complex, more rigid, and
obligate social structure.
An alternative hypothesis could be that the presence or
absence of a parent during development may affect tree
skink behaviour. As neither of our rearing treatments
included parents due to logistical constraints (see Methods
section), any potential effects of removing a parent were
not quantified. In the wild, the most common tree skink
social group does consist of parents and offspring (Bon-
nett 1999; Duckett et al. 2012). Although both juveniles
and adults can be found alone, social groups can also
consist of adults only, juveniles only, or parents and
offspring (Bonnett 1999; Duckett et al. 2012, Riley pers
obs 2016). In fact, in multiple Egernia group sp., off-
spring benefit from the presence of parents and gain
added protection, closer to optimal thermoregulation, and
increased access to prey (O’Connor and Shine 2004;
Langkilde et al. 2007; Sinn et al. 2008). Thus, as off-
spring benefit from the presence of parents in Egernia
group sp., one might expect there could be parental
effects on offspring behaviour. It is still unknown whether
juveniles benefit from the presence of parents in E. stri-
olata, yet it is an aspect to consider in the early devel-
opment of behaviour of this species.
Although our study did not find any evidence that social
isolation negatively affects spatial learning in tree skinks,
there are other lizard behaviours that could be affected by
social isolation. Personality traits and an individual’s
ability to interact with conspecifics are known to be altered
by social environment during development in mammals
and birds (Harlow et al. 1965; Naguib et al. 2011).
Hatchling veiled chameleons (Chameleo calyptratus)
raised in isolation were more submissive when interacting
with conspecifics and took longer to attack prey in a for-
aging task (Ballen et al. 2014). However, adult C. calyp-
tratus are largely intolerant of conspecifics (De Vosjoli and
Ferguson 1995, pp. 81–89), so our understanding of social
environment on lizard behaviour would benefit from fur-
ther research on a known social species. Social isolation
may also hinder the ability an individual has to process and
interpret social cues and information. Thus, isolation may
affect social learning ability because lack of social cues
during development may obstruct information transfer
between conspecifics. While we found no effect of social
isolation on individual learning ability, the same may not
be true of social learning and warrants further
investigation.
As the sociality of reptiles is becoming increasingly
recognized (Doody et al. 2012; Gardner et al. 2015), it is
crucial to also study the consequences and impact that
being social has on reptilian behaviour, ecology, and evo-
lution. Understanding the consequences of sociality for
reptiles is practically important for captive research,
breeding programs, and conservation. Management, con-
servation, and research programs may need to implement
group housing of social species to reduce potential negative
impacts of isolation on these animals’ development. Our
study did not find any evidence that social isolation nega-
tively affects spatial learning ability in the social tree skink.
However, more research is required to better understand
the negative effects of social isolation on other behavioural
and learning traits of this species. Because lizards have
relatively rudimentary parental care and species vary from
mainly solitary to highly social, they may represent a
unique opportunity to easily manipulate early social envi-
ronment and examine how behavioural development can be
shaped by sociality.
Acknowledgements We thank G. While and M. Favre for their
assistance in the field and laboratory, as well as J. Baxter-Gilbert and
F. Kar for their artistic and statistical advice.
Funding Financial support for this research was provided by the
Australian Research Council (DP130102998, awarded to MJW and
RWB), Natural Sciences and Engineering Research Council of
Canada (scholarship to JLR), the Australasian Society for the Study of
Animal Behaviour, the Australian Museum, and Macquarie Univer-
sity. DWAN was supported by an ARC Discovery Early Career
Research Award (DE150101774) and UNSW Vice Chancellors
Fellowship.
Compliance with ethical standards
Conflict of interest All the authors declare they have no conflict of
interest.
Ethical approval We followed guidelines for the care and use of
animals as laid out by the Association for the Study of Animal
Behaviour. Experimental protocols were approved by the Macquarie
University Animal Ethics Committee (ARA # 2013/039). Collection
of skinks was approved by the New South Wales National Parks and
Wildlife Service, Office of Environment and Heritage (License #
SL101264). Female skinks were captured either by hand, noosing or
Eliot trap and were placed in cloth bags until they could be trans-
ported by vehicle to Macquarie University from Albury, New South
Wales, in an insulated box. We observed no injuries resulting from
our cognition experiment.
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