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FEATURED STUDENT RESEARCH PAPER
Bold New World: urbanization promotes an innate behavioral
trait in a lizard
James Baxter-Gilbert
1,2
&Julia L. Riley
1,2,3
&Martin J. Whiting
1
Received: 8 March 2019 / Revised: 7 June 2019 / Accepted: 12 June 2019
#Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
Urban environments are novel landscapes that markedly alter animal behavior. Divergence in behavior in response to urbaniza-
tion may provide advantages in navigation, exploiting resources, and surviving under a novel suite of selective pressures.
Relatively few studies, however, have identified population-level behavioral changes in response to urbanization that are not
confounded by rearing environment and prior experience (e.g., an urban upbringing). To address this, we used the Australian
water dragon (Intellagama lesueurii) to test whether populations under varying levels of urbanization (urban, semi-natural, and
natural populations) differ in their innate behavioral traits; acquired either heritably or due to population-specific maternal effects.
Eggs were collected from wild mothers and hatched in the lab. Hatchlings were then reared in the lab under standardized
conditions (a common-garden experiment). We then assayed individual behavioral traits (boldness, exploration, and neophilia)
five times across their first year of development. We compared behavioral traits, as well as their expression (repeatability),
between urban, semi-natural, and natural populations. Neophilia and explorative behavior was similar among all populations.
However, dragons from semi-natural populations were significantly bolder than those from natural populations. Urban dragons
were also bolder than dragons from natural populations, although this trend was not significant because of high variance in
boldness. Dragons from semi-natural and urban populations had similar boldness scores, suggesting a potentially biologically
relevant difference in boldness between them and natural populations. We also saw some differences in the consistency of the
expression of behavior. Boldness in individuals from urban environments was also the only repeatable trait. Overall, our study
suggests that boldness is an innate, urban-derived divergent behavioral trait that likely contributes to the success of these lizards in
anthropogenically altered environments.
Significance statement
Lizards from human-modified areas are innately bolder than ones from natural habitats. To determine this, we raised lizards from
eggs collected from urban, semi-natural, and natural populations in a standardized environment, removing the effects of prior
experience and developmental environment, and examined their behavioral traits over time. The difference we found in boldness
was related to their origin population, rather than being shaped through experience, suggesting this trait may be heritable and is
being selected for in anthropogenic landscapes. Our study addresses an important gap in studies of urban behavioral ecology by
examining behavioral differences among replicated, differently urbanized, sites after experimentally accounting for both rearing
environment and prior experience.
Keywords Adaptation .Intellagama lesueurii .Personality .Urban ecology .Urban evolution
Communicated by T. Madsen
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s00265-019-2713-9) contains supplementary
material, which is available to authorized users.
*James Baxter-Gilbert
jx_baxtergilbert@laurentian.ca
1
Department of Biological Sciences, Macquarie University,
Sydney, New South Wales 2109, Australia
2
Department of Botany and Zoology, Stellenbosch University,
Stellenbosch 7600, South Africa
3
Ecology and Evolution Research Centre, School of Biological, Earth,
and Environmental Sciences, University of New South Wales,
Sydney, New South Wales 2052, Australia
Behavioral Ecology and Sociobiology (2019) 73:105
https://doi.org/10.1007/s00265-019-2713-9
Introduction
Novel landscapes can expose individuals to challenges that
may substantially alter their behavior (Sol et al. 2013;
Albertietal.2017;Lapiedraetal.2017). This action is
typified by the behavioral shifts of animals living within
urban environments (Shochat et al. 2006; Garroway and
Sheldon 2013;Lowryetal.2013; Sol et al. 2013), and
has been documented in birds (Atwell et al. 2012), insects
(Schuett et al. 2018), mammals (Lyons et al. 2017), reptiles
(Peterman and Ryan 2009), and spiders (Kralj-Fišer et al.
2017). These urban-derived divergent behaviors can in-
clude altered anti-predator responses (McCleery 2009;
Blumstein 2014), foraging behavior (Geggie and Fenton
1985;Shochatetal.2004; Short and Petren 2008), in-
creased problem-solving ability (Sol et al. 2011), behavior-
al thermoregulation (Peterman and Ryan 2009), and mate
communication (Parris et al. 2009;Barnett2015).
Furthermore, changes in behavioral traits (e.g., boldness,
neophilia, and exploration) may also provide advantages to
navigating and exploiting urban environments (Kralj-Fišer
et al. 2017). Boldness reflects an individual’s propensity to
take risks; bolder individuals may be more active in novel,
urban landscapes and situations, which could increase their
time spent foraging, mate searching, or defending a terri-
tory (Réale et al. 2007; Sol et al. 2013; Sprau and
Dingemanse 2017). Similarly, neophilia—an individual’s
willingness to engage with novel stimuli or objects—
could provide substantial advantages within an urban en-
vironment by increasing their ability to exploit novel re-
sources (e.g., food sources or shelter; Bókony et al. 2012;
Miranda et al. 2013). Finally, an individual’s propensity to
explore could influence their success in urban environ-
ments by increasing their ability to disperse across novel
landscapes (Damas-Moreira et al. 2019) and to gather im-
portant environmental information (e.g., identifying
refuge, basking, and perching locations in novel
environments; Lapiedra et al. 2017).
Although altered behavior and behavioral traits have been
documented in numerous urban-living species, the specific
mechanisms driving the formation of urban-derived divergent
behavioral traits are largely unclear (but see Miranda et al.
2013). Behavioral plasticity has been suggested to aid urban-
dwelling individuals increase their exploitation of urban re-
sources and decrease the costs associated with urban habitats
(Ditchkoff et al. 2006;Parteckeetal.2006;Frenchetal.2008;
Atwell et al. 2012;LucasandFrench2012; Lampe et al. 2014;
Kralj-Fišer et al. 2017). Alternatively, if these behavioral traits are
heritable, and provide an advantage in urban environments, then
selection may favor them in urban populations. Recent research
has suggested that urban evolution is driving the persistence of
species in heavily human-modified habitats (Johnson and
Munshi-South 2017). Yet, even though divergent behavior in
urban-living populations is likely adaptive, it is unclear if these
behaviors are a result of selection or plasticity (Diamond 1986;
Møller 2008;Lowryetal.2013;Soletal.2013; Alberti et al.
2017). Recently, heritability of behavioral traits (e.g., boldness
and aggression) has been documented for several urban-dwelling
bird species (Evans et al. 2010;Mülleretal.2013;Holtmann
et al. 2017; Sprau and Dingemanse 2017). Flight-capable birds,
however, should experience weaker selection within urban envi-
ronments compared with terrestrial species, because they are able
to rapidly vacate urban habitats leading to increased gene flow. In
contrast, less vagile terrestrial species are physically tied to spe-
cific locations within urban environments (Brown 1978;Wiens
and Donoghue 2004;Lyonsetal.2017), and thus may experi-
ence stronger selection. Research into heritable behavioral traits
in terrestrial urban species remains rare (but see Kralj-Fišer and
Schneider 2012), but they are a study system that could greatly
enhance our understanding of the full extent to which urban
environments are shaping animal behavior.
The Australian water dragon (Intellagama lesueurii)is
an agamid lizard species found throughout eastern
Australia (Cogger 2014). Water dragons are common in
urban areas and appear to have successfully exploited
human-altered landscapes, where some populations have
experienced rapid morphological evolution (Littleford-
Colquhoun et al. 2017). This species is therefore a good
model for testing whether behavior may play a role in
their success in urban environments. Specifically, we used
a common garden experiment, which removed the con-
founding effects of rearing environment and prior experi-
ence, to test whether urban environments are favoring
particular heritable behavioral traits or whether behavior
is best explained by experience. We raised hatchling
dragons from eggs collected from mothers living in urban,
semi-natural, and natural populations, and repeatedly
quantified their behavioral traits (boldness, neophilia,
and exploration) over the first year of life. We predicted
higher levels of boldness, neophilia, and exploration in
individuals from urban and semi–natural origin popula-
tions compared with their natural-living counterparts. If
these predictions are upheld, this would constitute evi-
dence for heritable behavioral divergence in urbanized
populations. We also examined if behavioral traits were
repeatable throughout development, and compared their
consistency among origin population categories (urban,
semi-natural, and natural). Repeatability of behavioral
traits across time suggests strong, constant selection for
a particular behavioral type within an environment
(Dingemanse and Réale 2005;Bell2012)andmaygive
an indication of broad heritability of a trait (Dohm 2002).
In contrast, lack of repeatability of behavioral traits may
indicate plasticity; which may be beneficial in order to
cope with changing, novel environments (Lampe et al.
2014; Griffin et al. 2016).
105 Page 2 of 10 Behav Ecol Sociobiol (2019) 73:105
Methods
Study species
Australian water dragons are a large (maximum snout-vent
length: 304 mm; Thompson 1993) agamid lizard. They are rela-
tively long-lived species (28–40 years; Harlow and Harlow
1997;Griffiths2006) with a generation time of 5 years
(Littleford-Colquhoun et al. 2017). They are naturally found in
forested areas associated with creeks, rivers, and other freshwater
bodies (Cogger 2014); however, they are also common in urban
parklands and other green spaces (Littleford-Colquhoun et al.
2017). These lizards are a dietary generalist (Baxter-Gilbert
2014), and are known to exploit anthropogenic food sources in
urban areas (Baxter-Gilbert 2018).
Field collection and husbandry
In the spring (October and November) of 2015, we collected
gravid female water dragons from 12 sites (four urban, four
semi-natural, and four natural) within a 50-km radius within
the greater Sydney area in New South Wales, Australia (see
Supplementary Materials for exact location details, sample
sizes, and SM Fig. 1). Urban sites had a dense local human
population and a landscape that was widely human-modified
(e.g., concrete, buildings, gardens, roads). Semi-natural sites
were protected green spaces (national and regional parkland)
that contained waterways adjacent to urban areas, and they
had a moderate human presence (park visitors). Natural sites,
although not completely free from human disturbance, were
generally associated with native bushland, waterways with
treed shorelines, and a relatively low human presence.
Upon capture, we transported females to Macquarie
University (Sydney, NSW), or if captured at Taronga Zoo
(Sydney, NSW) they were held there, and then oviposition
was induced (for egg collection details see Baxter-Gilbert
et al. 2018). Clutches of eggs were identically incubated
throughout development (at a constant temperature of
26.5 °C allowing for an equal sex-ratio; Harlow 2001).
Upon emerging, hatchlings were marked using a passive inte-
grated transponder (PIT) tag and randomly allocated to one of
15 common garden enclosures (approximately 6–7 lizards per
enclosure; initial experimental group N= 97 but group size
varied over time due to seasonal differences in capture suc-
cess; Table 1). The outdoor enclosures (6.2 m
2
plastic tubs
lined with sand, and containing tile refuges, hardwood dowel
perches, and a small pool) were contained within a predator-
exclusion net, which allowed for natural weather and photo-
periods common to the Sydney region (see SM Fig. 2).
Throughout the experiment, all dragons experienced identical
housing, husbandry conditions (fed vitamin-supplemented
crickets 3 times weekly), thermal conditions, and water ad
libitum.
Behavioral assays
We assayed three behavioral traits (exploration, boldness, and
neophilia) five times over the dragons’firstyearoflife(once
every 2 months, excluding the winter brumation period of July
and August). Dragon body size (snout-vent length) varied over
this time period, averaging 48 mm (± 0.19 standard error (SE),
min = 39 mm, max = 53 mm) initially, and growing to an aver-
age of 82 mm (± 1.21 SE, min = 64 mm, max = 133 mm) at the
end of the year. Behavioral trait assays were conducted indoors
over 3 days, and consisted of 1 assay per day. During each of the
five rounds of assays, we were not always able to re-capture all
lizards, resulting in some variation in sample sizes (Table 1). Our
experimental room was not large enough to house all dragons at
once, so we conducted assays in four batches (maximum of 32
individuals per batch, two batches per day, and 6 days total).
Assays took place in a temperature-controlled room, set to the
dragon’s preferred body temperature of 30 °C (Hosking 2010),
unless otherwise stated. During assays, dragons were individu-
ally housed and behaviors were remotely video recorded using a
security camera system (CCTV Security Systems, Melbourne,
Victoria). Each behavioral assay (exploration, boldness, neophil-
ia) was scored from the videos by a single researcher to ensure
consistency, with the video scorer being blind to the lizard’s
origin population (see below for scoring criteria).
Day 1: Explorative behavior
Our measure of explorative behavior quantified the amount of
time (s) a dragon spent moving (i.e., exploring) in a novel
arena. To assay these behaviors, we introduced dragons into
a novel environment, similar to an open-field test (Perals et al.
2017; Riley et al. 2017; Damas-Moreira et al. 2019). The
testing arenas were always the same size (rectangular arenas;
690 W × 470 L × 455 H mm) and had two black refuge boxes
(120 W × 175 L × 38 H mm) at opposite ends. We varied the
substrate between each of the five repeated measures (plain
paper, eucalyptus mulch, sugar cane mulch, topsoil, and pine-
bark mulch; see SM Fig. 3A) to ensure the arena was novel
each time. At the beginning of each trial, we introduced the
dragon into the arena within a central, containment refuge.
Table 1 Number of Australian water dragons (Intellagama lesueurii)
sampled for each round of behavioral assays split across each type of
origin population (natural, semi-natural, and urban)
Origin site type Round 1 2 3 4 5 All rounds
Natural 20 20 16 15 12 83
Semi-natural 49 51 45 43 40 228
Urban 28 26 25 24 23 126
All dragons 97 97 86 82 75
Behav Ecol Sociobiol (2019) 73:105 Page 3 of 10 105
The dragon was allowed to acclimate within this refuge for
5 min, whereupon the refuge was lifted, and the assay began.
Each exploration assay ran for 30 min. The dragons then
remained in these enclosures for the duration of the assay
period (3 days). From video recordings, we scored the time
a lizard spent moving within the trial (s). This value was used
as our “exploration score”; as the value increases, it reflects
more explorative behavior (Riley et al. 2017; Damas-Moreira
et al. 2019).
Day 2: Boldness
Our measure of boldness was the amount of time (s)ittooka
dragon to leave an unfavorable refuge after a simulated pred-
atory attack. We created a thermal difference within the testing
arena by lowering the temperature in the experimental room to
22 °C, and positioning a heat lamp directly over one of the
refuge boxes, creating a “hot”refuge (Carazo et al. 2014;
Riley et al. 2017; Damas-Moreira et al. 2019). We also posi-
tioned an ice pack beneath the enclosure, directly under the
other refuge, creating a “cold”refuge (Carazo et al. 2014;
Riley et al. 2017; Damas-Moreira et al. 2019;seeSM
Fig. 3B). By doing this, we created a high- and low-quality
refuge. At the beginning of each trial, we introduced the drag-
on into the arena within a central, containment refuge and left
it to acclimate for 5 min. We then simulated a predatory attack
by removing the containment refuge and “chasing”the dragon
with a blue, gloved hand until it entered the “cold”refuge
(Riley et al. 2017; Damas-Moreira et al. 2019). We then re-
motely video recorded the dragon’sbehaviorfor1h.Wemea-
sured a lizard’s boldness as the amount of time (s)ittookthe
dragon to leave the “cold”refuge. This value was our “bold-
ness score”, with lower times indicating higher boldness. If
the dragons did not exit the refuge within the duration of the
trial, we assigned it a value of 3600 s.
Day 3: Neophilia
Our neophilia assay quantified how close (cm) a dragon
would approach a novel object. Within each enclosure, a
bullseye (10-, 20-, 30-, and 40-cm diameter rings surrounding
a central 5-cm diameter circle) was printed on paper and taped
to the base of the arena (prior to all behavioral assays begin-
ning; see SM Fig. 3). The two refuge boxes from the previous
assay were removed, and a novel object was placed at the
center of the bullseye (see SM Fig. 3C). During the five neo-
philia assays, each individual saw a different novel object each
time. The objects chosen are common refuse items found in
urban areas that were similarly sized (between 6 and 8 cm
diameter), and was different across each assay period. The
novel objects were presented in this order: (1) unused 350-
ml paper coffee cups, (2) unused aluminum 160-ml pie tins,
(3) empty 600-ml water bottle, (4) unopened bag of 19-g
potato chips, and (5) unopened 330-ml soft drink can.
Similar to the previous two assays, each dragon was placed
within a central containment refuge at the start of an assay, and
left for 5 min to acclimate. To begin the assay, the central
containment refuge was removed, and individuals were left
for 30 min to interact with the novel object.
From the videos of the neophilia assay, we noted the prox-
imity of the individual to the novel object using the rings of
the bullseye to indicate distance to the object (e.g., outer-most
ring = 20 cm and inner-most ring = 5 cm). Dragons that
climbed the novel object were given a score of 0 cm, and
individuals beyond the outermost ring were assigned a score
of 25 cm. The closest distance a dragon approached the novel
object over the 30-min period represented its “neophilia
score”and was the value used in our analysis; lower scores
indicate a higher level of neophilia.
Statistical analyses
Behavioral traits
Before analysis, we explored our data following the protocol
detailed in Zuur et al. (2010). Two of our three behavioral
traits, boldness and neophilia, followed a normal distribution
and had no outliers. We used a rank transformation to normal-
ize our exploration score (Kar et al. 2016). Before analyses,
we also ensured there was no strong collinearity between
model predictor variables (i.e., a R
2
of greater than 0.70).
We examined differences in dragon behavioral traits using
linear mixed effect models (LMM, using the function lmer in
the lme4 R package; Bates et al. 2015;RCoreTeam2016).
We ran separate LMMs for each of the three behavioral traits.
The LMMs with exploration and neophilia as the response
variable included the fixed effects of dragon age (days since
hatching; continuous), origin population type (categorical:
natural, semi-natural, or urban), and batch (categorical: 1, 2,
3, or 4). The LMM with boldness as the response variable had
the additional continuous fixed factor of time spent scaring the
lizard (s). Continuous fixed factors were mean-centered using
az-transformation before analysis, which standardizes the var-
iables and facilitates interpretation of main effects in the pres-
ence of interactions (Schielzeth 2010). In all LMMs, we
accounted for dependencies within our data from sampling
each lizard repeatedly (random intercept and slope for lizard
identity across age), sampling individuals from the same
clutch (random intercept for lizard clutch), the same captive
enclosures (random intercept for tub identity), and the same
study population (random intercept for study site). To allow
comparisons among all origin site types, we re-leveled the
reference for origin population category and re-ran the model
(Nakagawa 2004). The assumptions of normality of residuals,
for both fixed and random effects, and heterogeneity of vari-
ance were verified for all LMMs (Zuur et al. 2009), αwas set
105 Page 4 of 10 Behav Ecol Sociobiol (2019) 73:105
at 0.05, and the R function confint was used to bootstrap 95%
confidence intervals for parameter estimates. We also calcu-
lated unconditional means and 95% CIs (corrected for non-
independence) for each origin population type using the func-
tion Effect in the R package effects (Fox 2003; Fox and Hong
2009). Assessment of unconditional means and the magnitude
of their differences (i.e., effect size) can reflect biological sig-
nificance (Nakagawa and Cuthill 2007; Gerstner et al. 2017).
Consistency in behavior
We examined the consistency of an individual’s behavioral
traits to investigate if repeatability was affected by origin pop-
ulation type. To accomplish this, we first subset the data by
origin population category, resulting in three separate datasets.
For urban-origin dragons, we had 126 observations from 28
individuals across 17 clutches, 14 enclosures, and 4 popula-
tions. For semi-natural-origin dragons, we had 225 observa-
tions of exploration, and 228 observations of boldness and
neophilia from 52 individuals across 32 clutches, 15 enclo-
sures, and 4 populations. For natural-origin dragons, we had
82 observations of exploration, and 83 of boldness and neo-
philia from 23 individuals across 14 clutches, 13 enclosures,
and 4 populations.
We calculated adjusted repeatability (R
adj
|age; Biro and
Stamps 2015) for each origin population type while control-
ling for the same covariates that were within their respective
LMMs (Nakagawa and Schielzeth 2010; Biro and Stamps
2015). We calculated 95% confidence intervals by
bootstrapping the data 1000 times with the boot function from
the R package boot (Davison and Hinkley 1997; Canty and
Ripley 2017). R
adj
|age was considered significantly more than
what would occur by chance alone if the 95% confidence
intervals did not overlap 0. We compared R
adj
|age between
treatments by visually examining overlap between 95% CIs
and the R
adj
|age value for natural, semi-natural, and urban
sites. Being conservative, we considered a difference as sig-
nificant if the 95% CIs did not overlap. Theoretically, R
adj
|age
ranges between 0 (individuals never expressing the same trait
value over repeated measures) and 1 (individuals always
expressing the same trait value over repeated measures;
Nakagawa and Schielzeth 2010), although the average repeat-
ability observed in the field of animal behavior is 0.37 (Bell
et al. 2009).
Results
Behavioral traits
Exploration did not significantly differ among origin popula-
tion category (Table 2; comparison between semi-natural and
urban: β= 0.118, 95% CI = −0.612, 0.427, t=−0.444, P=
0.657), and neither did neophilia (Table 2; comparison be-
tween semi-natural and urban: β=−0.628, 95% CI = −
3.173, 2.130, t=−0.445, P= 0.656). Dragons that originated
from semi-natural sites were significantly bolder than natural
sites (Table 2). Boldness did not significantly differ between
urban and natural sites (Table 2), nor semi-natural and urban
sites (β= 10.810, 95% CI = −408.829, 448.212, t=0.048,
P= 0.962). However, both the semi-natural and urban dragons
exited the hide (the metric for boldness) about 8.3 min (492 s
and 502 s, respectively) sooner than individuals in the natural-
origin population category (Table 2;Fig.1).
Consistency in behavior
Explorative behavior of dragons was not significantly repeat-
able in any origin population (urban: R
adj
|age = 0.44, 95%
CI = 0, 0.68; semi-natural: R
adj
|age = 0.14, 95% CI = 0, 0.40;
natural: R
adj
|age = 0.02, 95% CI = 0, 0.45). Similarly, neophil-
ia of dragons was not significantly repeatable in any origin
population (urban: R
adj
|age = 0.05, 95% CI = 0, 0.34; semi-
natural: R
adj
|age = 0.06, 95% CI = 0, 0.30; natural:
R
adj
|age =0, 95% CI =0,0.45).
Dragons originating from urban populations had moderate
repeatability in boldness (R
adj
|age = 0.32, 95% CI = 0.02,
0.63), while boldness was not significantly repeatable in
dragons from semi-natural (R
adj
|age =0.18, 95% CI=0,
0.41) and natural (R
adj
|age = 0.25, 95% CI = 0, 0.61) popula-
tions. Repeatability was not different among origin population
types in any of the behavioral traits measured.
Discussion
We found that water dragons from semi-natural populations were
significantly bolder than those from natural-origin populations.
Also, a difference between urban and natural-origin populations,
although non-significant, trended in the same direction. We ex-
pected lizards to be bolder in relation to the extent of urbanization
experienced by their origin population (i.e., urban dragons to be
most bold, semi-natural dragons to be moderately bold, natural
dragons to be least bold). Interestingly, the parameter estimates
reflect this logic. The difference in boldness between urban and
natural populations (parameter estimates and effect sizes) was
actually slightly greater (by 10 s) than the difference in boldness
between semi-natural and natural environments (Table 2;Fig.1).
The lack of significance is likely a consequence of greater vari-
ance in boldness among individuals within the urban environ-
ment. We suggest that the difference in boldness between
dragons from urban and natural-origin population categories is
likely still biologically relevant, because both the semi-natural
and urban dragons exited the hide at approximately the same
time, which was substantially earlier than individuals in the
natural-origin population type.
Behav Ecol Sociobiol (2019) 73:105 Page 5 of 10 105
Table 2 Outcomes of linear mixed effect models testing if behavioral traits (exploration, boldness,
and neophilia) were affected by dragon origin site type (natural: NT, semi-natural: SN, and urban:
UB). If fixed factors were not included in the analysis, this is represented with three hyphens (---). If
an effect was significant (at an ∞of 0.05), it is bolded. Other abbreviations found below are as
follows: N
obs
means number of observations, N
ind
reflects the number of individuals, N
mom
reflects
the number of clutches, N
tub
is the number of housing enclosures the individuals came from, and
N
site
is the number of specific origin populations we sampled
Exploration Boldness Neophilia
N
obs
=433, N
ind
=103, N
mom
=63, N
tub
=15, N
site
=12 N
obs
=437, N
ind
=103, N
mom
=63, N
tub
=15, N
site
=12 N
obs
=437, N
ind
=103, N
mom
=63, N
tub
=15, N
site
=12
Fixed effects β2.5% 97.5% tP β2.5% 97.5% tPβ2.5% 97.5% tP
Intercept −0.046 0.512 0.391 −0.201 0.841 2520.372 2067.041 3014.053 10.155 < 0.001 10.859 7.100 14.018 6.871 < 0.001
Age −0.198 −0.289 −0.121 −4.488 < 0.001 −75.231 −196.861 34.867 −1.177 0.239 −2.652 −3.753 −1.601 −5.346 < 0.001
Origin (SN; ref. = N T) 0.194 −0.332 0.755 0.728 0.467 −491.589 −982.453 −43.196 −1.959 0.050 −0.157 −3.390 3.198 −0.097 0.923
Origin (UB; ref. = NT) 0.312 −0.328 0.969 1.055 0.291 −502.400 −1085.466 41.771 −1.797 0.072 0.471 −3.260 4.518 0.265 0.791
Batch (2; ref. = 1) −0.173 −0.524 0.194 −0.975 0.330 −337.156 −852.754 107.125 −1.431 0.152 3.747 0.565 6.641 2.470 0.014
Batch (3; ref. = 1) −0.223 −0.509 0.066 −1.501 0.133 −194.761 −608.259 222.427 −0.977 0.329 2.615 −0.089 5.249 2.016 0.044
Batch (4; ref. = 1) −0.170 −0.592 0.298 −0.778 0.436 −613.325 −1203.419 11.032 −2.106 0.035 −1.112 −4.929 2.348 −0.559 0.576
Time spent scaring --- --- --- --- --- 277.775 153.078 392.119 4.413 < 0.001 --- --- --- --- -- -
Random effects σ
2
2.5% 97.5% σ
2
2.5% 97.5% σ
2
2.5% 97.5%
Identity (intercept) 0.382 0.170 0.517 208,640.400 31,915.713 512,528.290 0.269 0.001 9.197
Age (slope) 0.216 0.054 0.332 65,675.700 60.913 248,259.968 5.541 0.193 14.590
Clutch (intercept) 0.291 0.000 0.470 269,941.700 0.000 508,816.130 9.788 0.006 17.687
Tub (intercept) 0.000 0.000 0.255 6674.700 0.000 88,672.273 0.000 0.000 4.203
Site (intercept) 0.306 0.000 0.508 0.000 0.000 102,263.299 0.013 0.000 5.552
Residual 0.763 0.692 0.819 1,060,541.800 886,950.857 1,263,617.613 79.914 64.496 90.495
105 Page 6 of 10 Behav Ecol Sociobiol (2019) 73:105
Our findings support idea that wildlife persisting in, or
colonizing, urban environments have a tendency to be bolder
(reviewed in Lowry et al. 2013; Miranda et al. 2013; Sol et al.
2013) and suggests increased boldness in our urbanized water
dragons is innate, either as a heritable trait or because of ma-
ternal effects. These findings further align with recent studies
that demonstrate urbanization may be selecting for heritable
behavioral traits (e.g., increased aggression and boldness,
Evans et al. 2010;Mülleretal.2013;Holtmannetal.2017;
Sprau and Dingemanse 2017). If heritable, then increased
boldness in urban areas may promote fitness, through facili-
tating increased foraging and mating opportunities. This fit-
ness benefit may drive selection for enhanced boldness within
novel environments (Dingemanse and Réale 2005; Réale et al.
2007). The design of our common garden experiment was
able to remove a host of potential confounding factors, such
as nest environment, prior experience, or habituation (Evans
et al. 2010; Lampe et al. 2014; Vincze et al. 2016; Siviter et al.
2017), which does support our assentation that increased bold-
ness is an urban-derived heritable trait. Yet, we cannot rule out
the possibility of site-specific maternal effects. We recom-
mend future research into the behavioral traits of urban and
natural populations take into account any differences in the
allocation of nutrients and maternal hormones into developing
eggs, as this may alter hatchling behavioral traits (Groothuis
et al. 2005; Räsänen and Kruuk 2007; Bertin et al. 2009).
Maternal effects on behavioral traits may also include differ-
ences in maternal basking opportunities between populations,
as seen in other Australian agamids (Amphibolurus muricatus;
Schwanz 2016).
With respect to neophilia and exploration, we did not find
differences in among origin population categories. These behav-
ioral traits may not be strongly favored for within Sydney urban
environments. Alternatively, there may have been a flaw in the
trial design (e.g., testing arena size or means of measuring) or
there may be ontogenetic changes in the timing of expression of
these behaviors (e.g., perhaps dragons do not express variation in
neophilia or exploration behavior until they are older). Urban,
wild-caught brown anoles (Anolis sagrei) are bolder, less aggres-
sive, and more explorative compared with natural-origin popula-
tions (Lapiedra et al. 2017); however, in this study, they could not
rule out the effects of rearing environment and prior experience
on the behaviors they were observing. Expression of behavioral
traits like exploration and neophilia may be highly plastic in
urban habitats (Bókony et al. 2012; Sol et al. 2013). For example,
there is a positive correlation between boldness and aggression in
song sparrows (Melospiza melodia), but this relationship breaks
down in urban areas (Scales et al. 2011), which may result from
individuals modulating their behavior based on specific costs and
benefits associated with differing habitats (Sol et al. 2014).
Overall, more research is necessary to understand the selective
forces that are shaping the behavior of urban wildlife (Lowry
et al. 2013) and what determines the roles that both plastic and
fixed behavioral traits play for species persisting in urban
landscapes.
The only behavioral trait we observed to be consistent was
boldness in individuals from urban environments which was
significantly, but moderately, repeatable. Repeatability, or
consistency, in behavior across time generally reflects selec-
tion for the expression of that trait within that environment
−0.6
−0.4
−0.2
0.0
0.2
0.4
0.6 (a) Exploration
Unconditional Mean
NAT SEMI−NAT URB
1500
2000
2500
3000 (b) Boldness
NAT SEMI−NAT URB
9
10
11
12
13
14
15
16 (c) Neophilia
NAT SEMI−NAT URB
Fig. 1 Australian water dragons from semi-natural sites were significant-
ly bolder than those from natural sites (b). Here we present unconditional
means and 95% CIs of each behavioral trait, aexploration, bboldness,
and cneophilia, for each origin population category (black, gray, and
white points represent natural (NAT), semi-natural (SEMI-NAT), and
urban (URB) populations, respectively) of Australian water dragons
(Intellagama lesueurii)
Behav Ecol Sociobiol (2019) 73:105 Page 7 of 10 105
(Dingemanse and Réale 2005). For this reason, the repeatable
boldness in urban populations supports our assertion that ur-
ban selection favors consistently bolder individuals. For all
other behavioral trait and environment type combinations,
dragons exhibited low within-individual repeatability of be-
havioral traits, which suggests that plasticity in their expres-
sion may be favorable. However, an alternative hypothesis for
the general lack of repeatability in behavior is that the behav-
ior of juveniles may simply be more plastic (Favati et al. 2016;
Riley et al. 2017), with more fixed behaviors traits forming as
they mature. This would also suggest that rearing environment
and prior experience may inform the development of behavior
in these dragons. Formation of consistent behavior, related to
urban-derived behavioral syndromes, has been documented in
adult brown anoles (Lapiedra et al. 2017), and we suggest that
further research on adult dragon behavioral expression across
urban populations is required to determine if they would yield
comparable results. Potentially, practical issues with study de-
sign may be another explanation for why repeatability ofdrag-
on behavioral traits was not found across habitats and envi-
ronments. For example, we may have not selected an ecolog-
ically relevant time frame for the quantification of trait con-
sistency (Dohm 2002). Overall, further investigation into the
differences in behavior and the expression of behavioral traits
in anthropogenic landscapes will shed light into how selective
forces act on individuals during urban evolution.
In summary, urban landscapes are both expanding globally
and a major contributor to biodiversity loss (McKinney 2002;
Seto et al. 2012). In light of the novel landscapes humanity has
created (Ellis and Ramankutty 2008), it is imperative we un-
derstand the role of urban evolution in allowing wildlife to
adapt to an increasingly urban world (Dingemanse and
Réale 2005; Lowry et al. 2013;Holtmannetal.2017;
Johnson and Munshi-South 2017). Furthermore, we need to
understand how these naturally evolving divergent behavioral
traits can be applied to conservation actions and wildlife man-
agement to enhance our ability to protect species that are less
capable at persisting in urban areas, which is currently a major
threat to wildlife worldwide (Greggor et al. 2016). Our study
provides experimental evidence of an innate, urban-derived
divergent behavioral trait (boldness) in a vertebrate, removed
from the confounding effects of developmental environment
and prior experience, and advances our understanding of both
urban evolution (Johnson and Munshi-South 2017) and the
role of behavior in evolution, particularly in novel
environments.
Acknowledgments We would like to thank P. Bolton, C. Fryns, F. Kar, S.
Klopper, and D. Noble for their assistance in field. We are grateful to T.
Damasio, M. Mühlenhaupt, C. Wilson, and the husbandry volunteers at
Macquarie University’s Lizard Lab for their assistance in the lab, and P.
Harlow and O. Lapiedra for providing their insights into this topic.
Finally, we would like to thank the anonymous reviewers for their com-
ments and suggestions.
Funding This research was supported by scholarship from Macquarie
University (JBG) and Natural Sciences and Engineering Research
Council of Canada (JBG). JLR was supported by an Endeavor and
Claude Leon Foundation postdoctoral fellowship during this work.
Data availability The datasets generated during and/or analyzed during
the current study are not publicly available due to logistical constraints,
but are available from the corresponding author on reasonable request.
Compliance with ethical standards
Ethical approval for lizard captures and our experimental protocols
followed animal ethics guidelines that were approved by both the
Macquarie University Animal Ethics Committee (ARA no. 2015/023)
and Taronga Zoo Animal Ethics Committee (ARA no. 3b/08/15). Our
research was approved by the New South Wales National Parks and
Wildlife Service, Office of Environment and Heritage (License no.
SL100570).
Conflict of interest The authors declare that they have no conflict of
interest.
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