Different patterns of behavioral variation across and within species of spiders with differing degrees of urbanization

Abstract

Behavioral characteristics importantly shape an animals’ ability to adapt to changing conditions. The notion that behavioral flexibility facilitates exploitation of urban environments has received mixed support, but recent studies propose that between-individual differences are important. We leverage existing knowledge on three species of orb-web spider (Araneidae, Araneae) whose abundances differ along an urban–rural gradient to test predictions about between- and within-species/individual behavioral variation. We sampled Larinioides sclopetarius from their urban environment, and two species from suburban environments, Zygiella x-notata and Nuctenea umbratica. For each species, we quantified activity in a novel environment and within-species aggression. We analyzed between- and within-individual variation in behavior as well as their repeatability and correlations. As predicted, L. sclopetarius exhibited the highest activity in a novel environment and N. umbratica the lowest. Across all species, males were more aggressive than females and Z. x-notata was the most aggressive, followed by L. sclopetarius and N. umbratica. For all species, between-individual differences in activity and aggressiveness were repeatable; but the two behaviors were not correlated for any species. We next tested how group composition in relation to aggressiveness affects survival in high density conditions. Groups of Z. x-notata consisting of aggressive and tolerant spiders had higher survival rates than groups composed of only aggressive or tolerant individuals. Ultimately, we uncovered a complex pattern of behavioral variation between species as well as between and within individuals and we discuss the relative roles of this variation with respect to adapting to urban environments.

Significance statement
Urbanization has drastically changed biodiversity patterns. While the majority of species cope poorly with urban habitats, some species flourish in cities. Our understanding of behavioral characteristics that facilitate this exploitation, however, remains poor. We explored between and within species and individual variation in behaviors in ecologically similar orb-weaving spider species whose abundances differ along the urban–rural gradient. We detect both consistent individual differences and plasticity, in individuals’ response to a novel environment, suggesting that some degree of flexibility in reaction to novelty may be crucial in an urbanized environment. We also found that variation in aggressiveness type enables survival in high density conditions, conditions typical for urban populations. Urban populations thus exhibit a complex pattern of behavioral flexibility and behavioral stability.

Full text

ORIGINAL ARTICLE
Different patterns of behavioral variation across and
within species of spiders with differing degrees of urbanization
Simona Kralj-Fišer
1,2
&Eileen A. Hebets
3
&MatjažKuntner
1,4
Received: 16 February 2017 /Revised: 7 May 2017 /Accepted: 5 July 2017
#Springer-Verlag GmbH Germany 2017
Abstract
Behavioral characteristics importantly shape an animals’abil-
ity to adapt to changing conditions. The notion that behavioral
flexibility facilitates exploitation of urban environments has
received mixed support, but recent studies propose that
between-individual differences are important. We leverage
existing knowledge on three species of orb-web spider
(Araneidae, Araneae) whose abundances differ along an ur-
ban–rural gradient to test predictions about between- and
within-species/individual behavioral variation. We sampled
Larinioides sclopetarius from their urban environment, and
two species from suburban environments, Zygiella x-notata
and Nuctenea umbratica. For each species, we quantified ac-
tivity in a novel environment and within-species aggression.
We analyzed between- and within-individual variation in be-
havior as well as their repeatability and correlations. As pre-
dicted, L. sclopetarius exhibited the highest activity in a novel
environment and N. umbratica the lowest. Across all species,
males were more aggressive than females and Z. x-notata was
the most aggressive, followed by L. sclopetarius and
N. umbratica. For all species, between-individual differences
in activity and aggressiveness were repeatable; but the two
behaviors were not correlated for any species. We next tested
howgroupcompositioninrelationtoaggressivenessaffects
survival in high density conditions. Groups of Z. x-notata
consisting of aggressive and tolerant spiders had higher sur-
vival rates than groups composed of only aggressive or toler-
ant individuals. Ultimately, we uncovered a complex pattern
of behavioral variation between species as well as between
and within individuals and we discuss the relative roles of this
variation with respect to adapting to urban environments.
Significance statement
Urbanization has drastically changed biodiversity patterns.
While the majority of species cope poorly with urban habitats,
some species flourish in cities. Our understanding of behav-
ioral characteristics that facilitate this exploitation, however,
remains poor. We explored between and within species and
individual variation in behaviors in ecologically similar orb-
weaving spider species whose abundances differ along the
urban–rural gradient. We detect both consistent individual dif-
ferences and plasticity, in individuals’response to a novel
environment, suggesting that some degree of flexibility in
reaction to novelty may be crucial in an urbanized environ-
ment. We also found that variation in aggressiveness type
enables survival in high density conditions, conditions typical
for urban populations. Urban populations thus exhibit a com-
plex pattern of behavioral flexibility and behavioral stability.
Keywords Personality .Urbanization .Repeatability .
Behavioral types .Group composition
Communicated by J. Pruitt
Electronic supplementary material The online version of this article
(doi:10.1007/s00265-017-2353-x) contains supplementary material,
which is available to authorized users.
*Simona Kralj-Fišer
simonakf@gmail.com
1
Evolutionary Zoology Laboratory, Institute of Biology, Scientific
Research Centre of the Slovenian Academy of Sciences and Arts,
Novi trg 2, 1000 Ljubljana, Slovenia
2
Faculty of Mathematics, Natural Sciences and Information
Technologies, University of Primorska, Glagoljaška 8,
6000 Koper, Slovenia
3
School of Biological Sciences, University of Nebraska-Lincoln,
Lincoln, NE, USA
4
National Museum of Natural History, Smithsonian Institution,
Washington, DC, USA
Behav Ecol Sociobiol (2017) 71:125
DOI 10.1007/s00265-017-2353-x

Introduction
Behavior plays an important role in an animal’s ability to deal
with changes in its environment, including human-induced
changes (Shochat et al. 2006;Sihetal.2010;Tuomainenand
Candolin2011).While the vastmajority of speciesappear to cope
poorly with highly urbanized environments, certain species (e.g.,
fireants, pigeons, rats)flourishin cities (Karketal. 2007;Soletal.
2013) where they can reach extraordinarily high abundances in
city cores (McKinney 2002,2006). The life histories of these
Burban exploiters^are often characterized by rapid proliferation,
and a number of studies have begun to explore associated behav-
ioral characteristics that might facilitate urban exploitation. To
date, behavior of urban dwelling species has been explored at
predominantly three distinct scales—(i) across-species/popula-
tion behavior (inter-species/population variation); (ii) within-
species, between-individual behavior (between-individual vari-
ation); and (iii) within-species, within-individual behavior (with-
in-individual variation).
Acrossdifferent taxonomic groups,successfulurbanspecies
have been shown to exhibit reduced escape behavior, higher
aggression, and faster exploitation of novel resources as com-
pared to non-rural relatives (freshwater turtles: Trachemys
scripta elegans vs. Mauremys leprosa,Polo-Caviaetal.2008;
vultures: Coragyps atratus vs. Vultur gryphus, Carrete et al.
2010; several bird species, Sol et al. 2012,2013). Similarly,
within-species studies that compared conspecifics from rural
vs. urban populations revealedthat individuals from urban pop-
ulations tend to be more active and to exhibit more (albeit su-
perficial) exploration, reduced escape responses, increased
risk-taking behavior, and more aggression (eastern gray squir-
rel, Sciurus carolinensis, Partan et al. 2010; noisy miner,
Manorina melanocephala, Lowry et al. 2011;songsparrows,
Melospiza melodia,Scalesetal.2011;Capegroundsquirrel,
Xerus inauris, Chapman et al. 2012;15birdspecies,Møllerand
Ibáñez-Álamo 2012; reviewed in Miranda et al. 2013).
Additionally, a comparison of 20 bird species invading rural
and urban habitats found that birds from urban environments
tendedtohavea greater between-individual variation in aproxy
ofescapebehavior(i.e.,flightinitiationdistance)thantheirrural
conspecifics (Carrete and Tella 2011). These results and further
studiescorroborate the viewthat variation among individualsin
behavior traits may help explain a population’s ability to adapt
to urban environments (Sih et al. 2004,2010;reviewedin
Miranda et al. 2013).
Between-individual variation in behavior traits is increas-
ingly being studied to explain a population’s ability to adapt to
urban environments (Evans et al. 2010; Carrete and Tella
2011; Scales et al. 2011;Atwelletal.2012; Bókony et al.
2012; Carrete and Tella 2013; reviewed in Miranda et al.
2013). The co-existence of different behavioral types, in par-
ticular, may allow coping with a broad range of environmental
conditions, e.g., exploitation of diverse resources and niches
in urban environments (Møller 2010; Sih et al. 2010,2012;
Kralj-Fišer and Schneider 2012;Sih2013). Furthermore, in-
creased between-individual variation in behavior is expected
to result in higher functional diversity of species, e.g., aggres-
sive individuals may be good initial dispersers, whereas so-
cially tolerant individuals may cause population proliferation
(Fogarty et al. 2011; Sih et al. 2012). On the other hand,
constraints in behavioral expression within individuals may
be disadvantageous in unpredictable urban environments.
Interestingly, several studies that compared rural and urban
populations found that these differed in architecture of their
behavioral types; namely, rural individuals tended to exhibit
tighter correlations among behavior traits (e.g., behavioral
syndromes) as compared to urban conspecifics (Evans et al.
2010; Scales et al. 2011;Bókonyetal.2012; Miranda et al.
2013). This implies that the association between behavioral
traits may be more flexible in urban compared to rural species
or populations and potentially less constraining.
Despite a growing body of research examining the relation-
ship between behavioral traits and success at adapting to and
colonizing urban environments, the relationship remains un-
clear. While a certain degree of within-individual variability
(e.g., behavioral plasticity) is crucial to cope with
unpredictable/novel environments (Sol et al. 2013;Wong
and Candolin 2015), the same plasticity may also be maladap-
tive (Sinervo et al. 2010; Robertson et al. 2013;Wongand
Candolin 2015). Costs of plasticity may be Bevaded^through
behavioral streamlining, because different (stable) behavioral
types may do equally well when exposed to a range of (spa-
tially and temporary) different contexts (Watters and Sih 2005;
Cote et al. 2010; Sih et al. 2010; Fogarty et al. 2011;Wolfand
Weissing 2012). On the other hand, constraints in behavioral
responsiveness to environmental change would likely reduce
an individuals’ability to cope with urban environments. Thus,
the spread and maintenance of urban populations likely in-
volve a complex dynamic of between- and within-individual
variation in behavioral traits (Kralj-Fišer and Schneider 2012;
Sol et al. 2013; Halpin and Johnson 2014).
To date, behavioral characteristics of urban dwellers have
been mainly studied in birds and mammals (e.g., Evans et al.
2010; Møller 2010; Partan et al. 2010; Atwell et al. 2012;
Bókony et al. 2012; Bateman and Fleming 2014).
Surprisingly, arthropods remain largely underexplored in this
respect (but see Halpin and Johnson 2014), yet they represent
providers of important ecosystem services such as decompo-
sition, pollination, food web interactions, and biological con-
trol (Kotze et al. 2011). Additionally, due to their abundance
and short generation time, arthropods are good models to
study behavioral responses to urbanization (McIntyre 2000;
Niemelä and Kotze 2009; Kotze et al. 2011;Kralj-Fišer and
Schuett 2014). Arthropods also contain the archetypical urban
pests such as cockroaches, fleas, bed bugs, and others whose
spreading is medically and economically important.
125 Page 2 of 15 Behav Ecol Sociobiol (2017) 71:125

Among arthropods, orb-weaving spiders (Araneae,
Araneoidea) make particularly suitable organisms to study
characteristics of urban dwellers. Urbanized environments
provide web-building spiders’ample opportunities for build-
ing webs, and artificial light likely increases their foraging
success by attracting insects (Heiling 1999). City-dwelling
prey may also be available for an extended period in the sea-
son due to favorable urban temperatures (Heiling 1999;Kotze
et al. 2011), potentially increasing the spiders’reproductive
season and time to produce offspring. Indeed, a combination
of increased food availability and decreased predator exposure
may translate to higher fecundity, survival, and reproductive
output, as has been shown in the Australian golden orb weaver
Nephila plumipes (Lowe et al. 2014). However, other studies
found decreased reproductive rateand fecundity in individuals
inhabiting urban environments in Nephila clavata (Miyashita
1990) and in widow spiders Latrodectus hesperus (Johnson
et al. 2012), respectively, implying that only certain spider
species may adapt well to urban environments.
Here, we explore behavioral traits in three distinct species
of orb-weaving spiders (Family Araneidae) that each tends
to inhabit environments characteristic of different levels of
urbanization with varying success. Larinioides sclopetarius
represents a strictly urban species (i.e., urban exploiter)
(Kleinteich 2010; Kleinteich and Schneider 2011), whereas
Z. x-notata and N. umbratica inhabit both urban and more
pristine environments (Leborgne and Pasquet 1987;Bucher
and Entling 2011). Prior laboratory studies aimed to under-
stand why the three species differ in their success as city
dwellers found that L. sclopetarius exhibit high develop-
mental plasticity depending on food availability (e.g.,
growth rate, number of instars), a short life cycle (60 days
at ample food), and high reproductive output (up to 12 viable
egg cases, Kleinteich and Schneider 2011, our unpublished
data). Zygiella x-notata exhibits developmental plasticity
(growth rate, number of instars) and has intermediate devel-
opmental time (160 days at ample food, Mayntz et al. 2003)
and reproductive output (up to eight viable egg cases, our
unpublished data). Finally, N. umbratica showed a rather
canalized development, a long life cycle (240 days at ample
food, Kralj-Fišer et al. 2014), and comparably lower repro-
ductive output (up to four viable egg cases, our unpublished
data). We suspect that the combination of high food avail-
ability in urban environment and associated increased
growth through developmental plasticity and short genera-
tion times facilitate the successful exploitation of urban en-
vironments by L. sclopetarius and Z. x-notata. We also hy-
pothesize that differences in behavior exist both between
andwithinspecies.
We aimed to quantify and compare behavioral characteris-
tics of three species of spider that vary in their successful
establishment in urban envrionments. Specifically, we use
between-species and within-species comparisons of
L. sclopetarius,Z. x-notata,andN. umbratica to examine (i)
exploration of novel environments and (ii) aggression levels
with same-sex conspecifics. We assessed the relative contri-
bution of behavioral constancy and behavioral plasticity in
individuals’traits. We analyzed repeatability; i.e., proportion
of phenotypic variation (amount of within-individual vari-
ance) in a trait relative to the total phenotypic variation (sum
of within- and between-individual variance). Furthermore, we
examined potential individual differences in behavioral plas-
ticity in response to repeated novel environment test using
reaction norm approach (Dingemanse and Dochtermann
2013). Next, we examine the relationship between aggression
and high density living as it relates to survival. We do this by
using our calculations of aggression to artificially create high
density populations of N. umbratica and Z. x-notata (data
already exists on L. sclopetarius,Kralj-Fišer and Schneider
2012) whose composition consists of different behavioral
types, and we assess individual survival over time.
Given that a bold response to novelty has been repeatedly
shown as a key behavior determining animals’ability to dwell
in urban habitats (reviewed in Miranda et al. 2013), we predicted
L. sclopetarius—our most successful urban species—would ex-
press the highest activity levels. Concerning within-species ag-
gressiveness, we similarly expected higher levels of tolerance
towards conspecifics in L. sclopetarius and Z. x-notata—the
two species that naturally occur in aggregations—compared to
Bmore solitary^N. umbratica (e.g., Holway 1998).
In terms of the relationship between the composition of
aggressive individuals in high density populations and indi-
viduals’survival, prior work in L. sclopetarius found that
groups consisting of a balanced mix of aggressive and tolerant
individuals increased group survival (Kralj-Fišer and
Schneider 2012). Similar results, where groups composed of
individuals of mixed behavioral types outperformed monotyp-
ic groups, have been repeatedly found across diverse taxa
(Dyer et al. 2009;Coteetal.2010; Modlmeier et al. 2012;
Pruitt et al. 2012;Keiseretal.2014;Farineetal.2015;
Lichtenstein et al. 2016). As such, we expect that groups of
mixed aggression levels in both N. umbratica and Z. x-notata
will similarly experience the highest survival rates.
Methods
Study animals
Larinioides sclopetarius, commonly called the Bbridge
spider,^can be found across the Holarctic and is an extremely
successful colonizer of urban areas. High density populations,
which may count up to 100 individuals per m
2
(Burgess and
Uetz 1982; Heiling and Herberstein 1998;Schmitt2004;
Schmitt and Nioduschewski 2007a,2007b), tend to colonize
human urban constructions near bodies of water (Heiling and
Behav Ecol Sociobiol (2017) 71:125 Page 3 of 15 125

Herberstein 1998). These nocturnal spiders often build webs
adjacent to one another, but each web retains its full function-
ality (Heiling and Herberstein 1998). In areas inhabited by
bridge spiders, few other orb weawers can be found; they
are either entirely absent or limited to sporadic patches with
low population densities (Kleinteich 2010).
Zygiella x-notata, also distributed across the Holarctic, is an-
othersuccessfulcolonizer of urban areas.This speciescanbefound
onhuman constructions suchaswalls, fences, andwindowframes,
where they may be found in aggregations of up to 25 individuals
per m
2
(estimated from results of Leborgne and Pasquet 1987).
When found in the same habitat as L. sclopetarius,however,
L. sclopetarius dominates and appears to outcompete Z. x-notata
(Kleinteich 2010). In contrast to L. sclopetarius,Z. x-notata can be
found on urban vegetation (e.g., hedges, parks), on trees, and on
rocks in more pristine environments (Leborgne and Pasquet 1987;
Heiling and Herberstein 1998).
Nuctenea umbratica is a widespread central European spe-
cies. It is a habitat generalist that occurs in urban and pristine
environments. Individuals of N. umbratica appear to prefer land-
scapes with semi-open habitats, such as forest edge, hedgerows,
orchards, and single trees (Horváth and Szinetár 2002; Horváth
et al. 2005;Bucheretal.2010). When found in urban environ-
ments Nuctenea spiders inhabit trees, shrubs, or wooden con-
structions, where they build large orb webs. In cities,
N. umbratica often co-occurs with, and is outcompeted by,
L. sclopetarius and/or Z. x-notata (pers. obs.). Despite the fact
that these spiders are ubiquitous (Horváth et al. 2005), we never
observed them in large aggregations.
Species collections
We collected subadult L. sclopetarius males and females from
artificial constructions, e.g., buildings, fences, and bridges, along
riverbanks in two different locations in Hamburg, Germany
(53.577401, 10.009699), in September 2010. We collected
Z. x-notata subadults in May 2012 in suburban areas of Vipava
from man-made constructions along the Vipava riverbank (all
spiders were collected in one location), Slovenia (45.844605,
13.963604). We collected subadult N. umbratica spiders from
their webs on trees and hedgerows along the Ljubljanica river-
bank in suburban areas of Ljubljana (all spiders were collected in
one location), Slovenia (46.045093, 14.506048), between May
and July 2011. While Z. x-notata and N. umbratica were ob-
served in rural, suburban, and urban environments,
L. sclopetarius appeared only in urban areas. The density of in-
dividuals was the highest in L. sclopetarius,intermediateinZ. x-
notata,andthelowestinN. umbratica.
Field-collected subadults of all three species were transferred to
the closest laboratory (Germany, Slovenia), kept in 200-ml plastic
cups, and fed with fruit flies (Drosophila sp.). Individuals were
collected as subadults and then reared to adulthood in the labora-
tory to assure their virginity and thus the same mating status. Upon
maturation, adult females, which are larger than males across all
species, were transferred into plastic frames (36 × 36 × 6 cm) and
fed with blowflies (Calliphora sp.) The adult males of all species
cease web building upon sexual maturation, and were thus
retained in plastic cups with feeding treatment as in females.
Throughout the study, the spiders were kept at room temperature
under LD 10:14 conditions, fed two flies twice a week, and water-
sprayed 5 days a week. At maturity, we weighed all spiders (accu-
racy 0.01 mg) before subjecting them to experiments.
Experimental design
1. Between and within-species behavioral variation
We subjected spiders of all three focal species to two tests
for behavioral characterization: (i) a novel environment test
which measured behavior related to activity in a novel envi-
ronment (duration of initial activity when placed into the nov-
el environment); and (ii) a contest test which we used as a
proxy for aggressiveness towards a same-sex conspecific.
Using a repeated measures design in which each spider par-
ticipated in both tests twice, we observed 61 L. sclopetarius,
61 Z. x-notata,and85N. umbratica individuals. We addition-
ally repeatedly tested 10 additional N. umbratica spiders in the
novel environment test. The order of tests and of observed
individuals was chosen randomly. Though we aimed to test
all individuals twice in each of the test situations, this was not
always feasible due to death (Z. x-notata,N=3;N. umbratica,
N= 3). The spiders were always fed 1 day before testing, and
an individual was never observed more than once a day.
Unfortunately, it was not possible to record data blind because
our study involved observations of focal animals.
2. Activity in a novel environment
In order to quantify each spider’s activity level in a novel
environment, we carefully placed a test spider into an unfa-
miliar plastic container (11 × 11 × 6 cm) using a paintbrush.
Generally, the spider immediately started to move around the
container. In the next 5 min, we recorded the latency to the
first halt (hereafter termed duration of initial activity in a novel
environment; e.g., Kralj-Fišer and Schneider 2012).
3. Aggressiveness towards same-sex conspecific
To calculate an individual’s level of aggression with a same-
sex conspecific, we staged two individuals about 5 cm from each
other and recorded agonistic behavior for 20 min. Females were
tested twice in random order with 1 to 3 weeks in between—once
as residents in their own web and once as intruders on an unfamil-
iar web. Females usually reside in a retreat within a corner of the
web frame. For female–female interactions then, an Bintruder^
femalewasgentlyplacedintotheresidentwebwitha
125 Page 4 of 15 Behav Ecol Sociobiol (2017) 71:125

paintbrush. Male orb weavers cease web building after maturity.
Thus, to observe male intra-sexual aggressiveness, two males
were placed at the hub of a female web, approximately 5 cm from
each other, while the female was in her retreat. Males and females
were tested twice. No individual was paired with the same oppo-
nent more than once.
Aggressiveness was measured as a score based on the frequen-
cy of what we deem to be Baggressive^behavior: approaching
(score = 1), web-shaking (score = 1), attacking (score = 2), and
chasing (score = 3) (e.g., Kralj-Fišer et al. 2011;Kralj-Fišer and
Schneider 2012). Aggressive behaviors were similar for all three
species. BApproach^was defined as a movement by one spider
towards the other individual, Bweb-shaking^was defined as sud-
den and large amplitude shaking of the web, which spiders usually
exhibit when approaching another individual (Lubin 1980),
Battacking^is defined as a sudden move in the direction of the
other individual resulting in a body contact with the opponent,
andBchasing^is defined as arunningafter the (escaping) opponent
resulting in a successful attack or escape of the opponent. The sum
of these scores for each individual was used as its aggressiveness
score.
Statistical analyses
We first tested for inter-species differences in the behavioral
scores using a generalized estimating equation (GEE) which
allows for non-normal distribution and the repeated measures
(subject = id, within = sequence). We assessed sex and species
differences (independent variables) for each of the measured
behaviors (dependent variables: activity scores, aggressiveness
scores). We compared species and sexes using Wald chi-square
statistics with leastsignificantdifferenceadjustmentscorrecting
for multiple comparisons, where appropriate. We performed
these analyses in SPSS. We also performed Markov Chain
Monte Carlo Linear Mixed Model (MCMCglmm) analyses in
R (version 2.15.3, Core R Team 2013) with sex and species as
independent factors (Hadfield 2010); Supplement 1has R
scripts and results. In the next step, we analyzed between- and
within-individual variance of behaviors for each species sepa-
rately (intra-species behavioral variation). To test for the exis-
tence of distinct behavioral variation in activity level and ag-
gressiveness, we used the mixed-effect modeling approach
(Dingemanse and Dochtermann 2013). We primarily estimated
the degree to which the trait expression varies among individ-
uals (between-individual variance) and the degree to which the
trait expression varies within an individual (within-individual
variance), which we also used to calculate repeatability. High
between-individualvariancevs. low within-individual variance
in a trait expression implies the existence of stable individual
differences in the trait while the within-individual variance in-
forms on average plasticity in the expressed behavior.
We used the Markov Chain Monte Carlo Linear Mixed
Model (MCMCglmm) to estimate the sources of variation in
behavioral measures (dependent variables) and to analyze the
behavioral correlations (Dingemanse and Dochtermann 2013)
for each species separately. We performed these analyses in R
(version 2.15.3, Core R Team 2013) using the MCMCglmm
package (Hadfield 2010).
In order to decompose phenotypic variance to within- and
between-individual components, we included individual as ran-
dom effect in the model. To estimate the significance of between-
individual variance in intercept or elevation, we compared the
deviance information criterion (DIC) (Grueber et al. 2011)of
constrained (without random factor) and unconstrained models
(id as random factor), and assumed better fit of the model when
DIC constrained −DIC unconstrained >5. We added sex and test
sequence as fixed effects in the model and calcula ted the adjusted
repeatability with 95% confidence interval according to
Nakagawa and Schielzeth (2010). We applied Box-Cox to trans-
form data of initial activity in a novel environment (Box and Cox
1964; Osborne 2010) using MASS (Ripley et al. 2011). Scripts
are given in Supplement 2.
We used bivariate mix-effects modeling to assess behavior-
al correlations. We calculated phenotypic correlations be-
tween aggressiveness and initial activity following the ap-
proach suggested by Dingemanse and Dochtermann (2013).
We also partitioned out the between-individual correlations
from the phenotypic ones because a between-individual cor-
relation need not be captured effectively by the phenotypic
correlation; estimating the between-individual correlation
has been advised to be used in behavioral syndrome research
(Dingemanse and Dochtermann 2013). We compared DIC of
constrained (inter- and within-individual co-variances are set
to zero) and unconstrained models (within-individual co-
variance is set to zero) for a better fit. Both variables were
transformed with log function, because models with data be-
ing Box-Cox transformed appeared unstable. Scripts are given
in Supplement 3.
In the above analyses, individuals were treated as random
effects to allow individual variation in intercept. But since indi-
vidual reaction norm slopes vary due to variation in individual
phenotypic plasticity, we tested for individual variation in reac-
tion norm slopes by fitting additional MCMCglmms with differ-
ent random effect structures (Nussey et al. 2007). Model 1
allowed individual variation in intercept (between-individual
variance in intercepts = V
ind0
≠0) and common slopes across
all individuals (between-individual variance in
slopes = Var
ind1
= 0). Model 2 allowed individual variation in
intercept and slope (Vi
nd0
≠0, Var
ind1
≠0). Individuals exhibit
variation in phenotypic plasticity when model 2 receives better
support (lower DIC) than model 1. If model 1 received the lowest
DIC, this would suggest high between-individual variation in
behavior, but low variation in individual phenotypic plasticity.
We report results of model comparisons (DICs are given in
Table 3) together with the best fit, the model results for V
ind0
andVar
e
(=residual variance) aswellas Var
ind1
,when applicable.
Behav Ecol Sociobiol (2017) 71:125 Page 5 of 15 125

Composition of aggressiveness types in high densities
and survival
Wehave previously shown in L. sclopetarius that groups var ying
in the composition of individual aggressiveness type differ in
number of survivors under high density conditions (Kralj-Fišer
and Schneider 2012). Here we conducted similar experiments in
Z. x-notata and N. umbratica. According to the aggressiveness
scores, we composed three classes of groups: (i) aggressive
groups, (ii) non-aggressive groups, and (iii) mixed groups.
Each group consisted of seven adult individuals (five females
and two males), as this density has been previously shown to
result in cannibalistic events and/or starving (Kralj-Fišer and
Schneider 2012), thus creating a challenging environment for
these spiders. Aggressive groups were c omposed of spiders from
the upper third of the aggression score distribution (no. of groups:
Z. x-notata =6;N. umbratica = 6). Non-aggressive groups were
composed of spiders from the lower third of the aggression score
distribution (no. of groups: Z. x-notata =5;N. umbratica =6).
Finally, the mixed group was composed of randomly selected
spiders that had not gone through aggressiveness scoring (no.
of groups: Z. x-notata =5;N. umbratica = 7). All individuals
wereweighed a dayprior to theexperiment to assuresimilar body
sizes of individuals in the same group. Groups were housed in
terraria (36 × 36 × 6 cm) and were provided with identical prey
regimes (14 flies) twice a week. We checked for cannibalized
spiders three times per week, and removed remains of dead indi-
viduals. After 21 days, mortality and individual body weight of
surviving spiders were assessed.
Statistical analyses
Wetested forthe effect oftreatment(different groupcompositions:
aggressive, non-aggressive, mixed) on the estimated individual
weight changes, (final average individual mass−start average individual mass
start average individual mass ),
and the number of survived spiders using Kruskal-Wallis tests.
The average individual weight was used since we could not iden-
tify individual spiders after 21 days. We used the Mann-Whitney
Utest when comparing two groups.
Results
Between and within-species behavioral variation
Between-species behavioral variation
1. Activity in a novel environment
The three species differed in the duration of initial activity in a
novel environment (species: Wald χ
2
= 37.142, df = 2, P< 0.001;
sex: Wald χ
2
=0.087,df=1,P= 0.768; species*sex: Wald
χ
2
= 4.928, df = 2, P= 0.085; N= 217; Table 1;Fig.1). As
predicted, L. sclopetarius were active for the longest period in
the novel environment and Nuctenea umbratica exhibited the
shortest activity (Table 1). The duration of activity in
L. sclopetarius was not significantly higher than in Z. x-notata
(Table 1;Fig.1).
We found no between-sex differences in duration of initial
activity in a novel environment in any of the three species;
however, individuals differed significantly in duration of ini-
tial activity when placed in a novel environment for the first
vs. second time (Table 2). While L. sclopetarius spiders in-
creased activity durations, Z. x-notata and N. umbratica ex-
hibited shorter activity in their second trial (Table 2).
2. Aggressiveness towards same-sex conspecific
Theaggression scores differedamongspecies, sexes, andtheir
interaction (species: Wald χ
2
= 46.494, df = 2, P<0.001;sex:
Wal d χ
2
= 93.949, df = 1, P< 0.001; species*sex: Wald
χ
2
= 1.208, df = 2, P= 0.547; N= 207). Across all species, males
were more aggressive than females (mean difference = 14.18,
SE = 1.799, P< 0.001). The most aggressive species were Z. x-
notata, followed by L. sclopetarius, and the least aggressive were
N. umbratica (Table 1;Fig.1). The aggressiveness levels did not
differ between the two repeated trials (Table 2).
Within-species behavioral variation
1. Activity in a novel environment
We found significant between-individual variances in ini-
tial activity in L. sclopetarius (range = 1.8–298.23), Z. x-
notata (range = 0–298.5), and N. umbratica (range = 0–
95.44), i.e., DICs of constrained (without random factor)
models were higher from DICs of unconstrained models (id
as random factor) (Table 2). The individual differences in
initial activity in a novel environment were significantly re-
peatable in L. sclopetarius (mean r= 0.493); Z. x-notata
(mean r= 0.426), and N. umbratica (mean r= 0.481)
(Table 2; Fig. 2).
2. Aggressiveness towards same-sex conspecific
The between-individual variation in aggressiveness was sig-
nificant in all three species (L. sclopetarius,range=0–76; Z. x-
notata,range=0–95; and N. umbratica,range=0–94 Table 2).
The individual differences in intra-sex aggressiveness appeared
significantly repeatable, with the mean repeatability estimates
0.832, 0.838, and 0.781 in L. sclopetarius,Z. x-notata, and
N. umbratica, respectively (Table 2;Fig.2).
125 Page 6 of 15 Behav Ecol Sociobiol (2017) 71:125

Variation in individual phenotypic plasticity
Model 2, which included individual variation in intercept and
slope, received better support than model 1, which included
individual variation in intercept only (L. sclopetarius, m2:
V
ind0
= 0.168, Var
ind1
= 0.110; Var
e
= 0.048; Z. x-notata,
m2: V
ind0
= 0.149, Var
ind1
= 0.093; Var
e
= 0.027;
N. umbratica,m2:V
ind0
= 0.142, Var
ind1
=0.08;
Var
e
= 0.051; Table 3; Fig. 3). Namely, L. sclopetarius,Z. x-
notata, and N. umbratica exhibited individual variation in
phenotypic plasticity in initial activity in a novel environment.
In other words, individuals differed in the degree of change in
their activity levels when comparing their first exposure vs.
the second exposure to novel environment test. Comparably,
the results suggest that individuals exhibited high between-
individual variation but low variation in plasticity in aggres-
siveness (L. sclopetarius,m1:V
ind0
=1.53,Var
e
= 0.21; m2:
V
ind0
= 0.11, Var
ind1
= 0.34; Var
e
= 0.12; Z. x-notata, m1:
Var
ind0
=2.36,Var
e
=0.22;m2:V
ind0
=1.88,Var
ind1
=0.34;
Var
e
=0.22;N. umbratica,m1:Var
ind0
=1.82,Var
e
=0.31;
m2: V
ind0
=1.21,Var
ind1
=0.48;Var
e
=0.14).
Behavioral correlations
The unconstrained and the constrained models had very similar
DIC estimations. This implies thatthe between-individual and
phenotypiccorrelationsamong aggressivenessand initial activ-
ity in a novel environment were non-significant (results are
given in Table 4) in all tested species. See also Supplement 3.
Sequence 1 Sequence 2
Aggression score
Acvity in novel environment
1.3
1.1
0.9
0.7
1.3
1.1
0.9
0.7
L. sclopetarius
Z. x-notata
N. umbraca
0
20
40
60
80
100
0
20
40
60
80
100
Females Males
Fig. 1 Intra-sex aggressiveness scores and durations of initial activity in a novel environment (Box-Cox transformed) in the three tested species. The above
panels represent data from the first test (sequence 1), the below panels show data from the repeated test (sequence 2). Species differences are given in Table 1
Tabl e 1 Post hoc results of generalized estimating equation (GEE) testing for species differences in intra-sex aggressiveness (N= 207 individuals) and
duration of initial activity when placed in a novel environment (N= 217 individuals)
Species (1) Species (2) Mean difference Std. error df PLower 95%
Wald CI for diff.
Upper 95%
Wald CI for diff.
Initial activity in a novel environment
L. sclopetarius Z. x-notata 16.32 9.599 1 0.089 −2.48 35.15
L. sclopetarius N. umbratica 34.88 6.143 1 <0.001 22.84 46.92
Z. x-notata N. umbratica 18.55 7.620 1 0.015 3.62 33.48
Aggressiveness
L. sclopetarius Z. x-notata −7.17 2.261 1 0.002 −11.61 −2.74
L. sclopetarius N. umbratica 4.98 1.343 1 <0.001 2.34 7.61
Z. x-notata N. umbratica 12.15 2.078 1 <0.001 8.08 16.22
Significant results (after correction for multiple comparisons) are bolded. Similar results were given by MCMCglmm (see Supplement 1)
Behav Ecol Sociobiol (2017) 71:125 Page 7 of 15 125

Composition of aggressiveness types in high densities
and survival
We aimed to further test the importance of between-individual
variation in aggression for survival in high density conditions.
Higher numbers of N. umbratica vs. Z. x-notata spiders
survived under high density conditions for 3 weeks
(F
34,1
= 34.817, P<0.001;Fig.4). The average individual
mass at the end was higher than the average individual mass at
the start of high density experiment in N. umbratica
(Wilcoxon Z=−3.823, P<0.001,N= 19), but not in Z. x-
notata (Wilcoxon Z=−0.621, P=0.535,N=15;Fig.4).
Tabl e 2 Results of MCMCglmm
estimating variance components
of measured behaviors
(aggressiveness, latencies to stop
activity when placed into the
novel environment) with fixed
(sequence, sex) and random
effects (id)
Post. mean l-95% CI u-95% CI pMCMC
Aggressiveness
L. sclopetarius (Intercept) −0.732 −1.450 0.282 0.14
Sequence 0.202 −0.006 0.427 0.12
Sex 1.507 0.920 1.906 <0.01
Between-individual variance 0.996 0.553 1.620
Within-individual variance 0.237 0.119 0.345
Repeatability 0.832 0.679 0.930
Z. x-notata (Intercept) 0.356 −0.666 1.553 0.62
Sequence 0.076 −0.145 0.272 0.46
Sex 1.091 0.339 1.901 <0.01
Between-individual variance 2.172 1.320 3.307
Within-individual variance 0.340 0.156 0.547
Repeatability 0.838 0.763 0.942
N. umbratica (Intercept) −1.817 −2.732 −0.745 <0.01
Sequence 0.207 −0.025 0.427 0.14
Sex 1.660 1.103 2.178 <0.01
Between-individual variance 1.209 0.800 1.939
Within-individual variance 0.332 0.182 0.551
Repeatability 0.781 0.632 0.890
Initial activity in a novel environment
L. sclopetarius (Intercept) 2.057 1.795 2.314 <0.01
Sequence 0.118 0.040 0.195 <0.01
Sex 0.168 −0.011 0.322 0.08
Between-individual variance 0.082 0.034 0.134
Within-individual variance 0.068 0.052 0.099
Repeatability 0.493 0.339 0.692
Z. x-notata (Intercept) 1.122 0.932 1.402 <0.01
Sequence −0.141 −0.230 −0.062 <0.01
Sex −0.096 −0.221 0.037 0.12
Between-individual variance 0.024 0.007 0.055
Within-individual variance 0.049 0.037 0.085
Repeatability 0.426 0.107 0.592
N. umbratica (Intercept) 0.682 0.493 0.857 <0.01
Sequence −0.046 −0.107 0.002 0.10
Sex 0.058 −0.068 0.138 0.28
Between-individual variance 0.455 0.027 0.068
Within-individual variance 0.052 0.036 0.061
Repeatability 0.481 0.336 0.632
The significant effects of the fixed factors (P< 0.05) are bolded. To estimate the significance of between-
individual variance in intercept or elevation, we compared constrained (without random factor) and unconstrained
models (id as random factor), and defined significance when DIC (deviance information criterion)
unconstrained −DIC constrained <5. We calculated adjusted repeatability and their 95% credible intervals (CI).
Significant estimates are bolded. Detailed results are given in Supplement 1
125 Page 8 of 15 Behav Ecol Sociobiol (2017) 71:125

While we found no differences in survivorship between
group classes in N. umbratica when exposed to high density
conditionsfor 3 weeks (Kruskal-Wallis test, χ
2
=1.303,df=2,
P= 0.521), the group classes in Z. x-notata significantly dif-
fered in number of survived individuals (Kruskal-Wallis test,
χ
2
= 9.551, df = 2, P= 0.008; Fig. 4). In Z. x-notata, the
groups of mixed individuals had significantly higher survivor-
ship than groups consisting of only aggressive (Mann-
Whitney U=1,N=11,p= 0.009) or only non-aggressive
individuals (Mann-Whitney U=0,N=10,p= 0.007); how-
ever, there was no difference between aggressive and non-
aggressive groups (Mann-Whitney U=11,N= 10,
P= 0.841; Fig. 4).
While the change in average individual mass did not differ
among groups in N. umbratica (Kruskal-Wallis test,
χ
2
=0.853,df=2,N=19,P= 0.653), we found significant
differences between groups in Z. x-notata (Kruskal-Wallis
test, χ
2
=6.146,df=2,P= 0.046); namely, survivors in the
groups of aggressive individuals had decreased mass, in
groups of non-aggressive individuals survivors exhibited in-
creased mass, and in the mixed groups survivors did not
change the mass. The change in average individual mass dif-
fered significantly between aggressive and non-aggressive
groups (Mann-Whitney U=3,N=11,P= 0.03), but did
not differ between non-aggressive and mixed groups (Mann-
Whitney U=4,N=10,P= 0.095), or between aggressive and
mixed groups (Mann-Whitney U=9,N=11,P=0.329).
Discussion
In this study, we contrast behavioral variation among three
orb-web spider species that commonly occur along an urban
to suburban gradient: Larinioides sclopetarius, an urban ex-
ploiter, dominant in its habitat; Zygiella x-notata that mainly
dwells in human-altered areas; and Nuctenea umbratica that
lives on trees in urban and suburban environments. We com-
pared L. sclopetarius from urban areas to suburban Z. x-notata
and N. umbratica, and found these species to differ in their
average levels of activity in a novel environment and
Aggression score 1
Aggression score 2
Acvity in novel environment 1
Acvity in novel environment 2
1.4
0.7
0.7 1.4
0
20
40
60
80
100
020 40 60 80
L. sclopetarius
Z. x-notata
N. umbraca
L. sclopetarius
Z. x-notata
N. umbraca
Fig. 2 Aggressiveness scores (above) and durations of initial activity in a
novel environment test (Box-Cox transformed) (below), in the first and
second repeats in L. sclopetarius,Z. x-notata,andN. umbratica.Results
are given in Table 2
Tabl e 3 Deviance information
criteria of candidate models L. sclopetarius Z. x-notata N. umbratica
Aggressiveness
Model 1: random = ~ID 654.65 682.24 726.30
Model 2: random = ~idh(1 + sequence):ID 655.87 682.54 726.92
Initial activity in novel environment
Model 1: random = ~ID 71.55 21.82 105.76
Model 2: random = ~idh(1 + sequence):ID 51.21 9.10 94.21
All models were fit with sequence number as a fixed effect, and differ in their random structure. Model 2 includes
common slopes but allows individualvariation in intercepts; model 2 allows individual variationin intercept and
slope. The models with the lowestDIC are bolded. Individuals exhibit individual variation in behavioral plasticity
when model 2 receives better support. In case that model 1 receives the lowest DIC, data suggest high between-
individual variation in behavior, but low individual variation in behavioral plasticity
Behav Ecol Sociobiol (2017) 71:125 Page 9 of 15 125

aggressiveness, but to exhibit similarities in relation to within-
and between-individual variation in behavior.
Comparing species average behavior levels, we detected
that L. sclopetarius exhibited the highest activity in the novel
environment and N. umbratica the lowest, while Z. x-notata
exhibited intermediate activity. Scientists often equate an an-
imal’s reaction to novelty, such as a novel environment, to its
boldness, e.g., in response to predator exposure (Huntingford
1976;BellandStamps2004; Kortet and Hedrick 2007).
Boldness, in turn, is hypothesized to enable an organism to
adapt to urban environments (reviewed in Miranda et al.
2013). Indeed, research on other organisms has found that
individuals in urban populations exhibit reduced fear of novel
stimuli as compared to those in rural populations (e.g., Passer
domesticus, Martin and Fitzgerald 2005;Acridotheres tristis,
Sol et al. 2011; reviewed in Miranda et al. 2013), supporting
the idea that boldness might enable adaptation to urban
Fig. 3 Durations of initial activity (Box-Cox transformed; y-axis) in the first and repeated novel environment test (x-axis: 1 and 2) in L. sclopetarius,
Z. x-notata,andN. umbratica.Lines represent individuals’reaction norm slopes
Number of survived females
Zygiella x-notata N. umbraca
5
4
3
2
1
0
Group composion
Aggressive individuals
Non-aggressive individuals
Random induviduals
Fig. 4 Boxplots represent data from the three different group
compositions (only aggressive individuals, only tolerant individuals,
random individuals) exposed to high density conditions for 21 days for
Z. x-notata and N. umbratica. Differences between group compositions in
the number of survived females: Z. x-notata (Kruskal-Wallis test,
χ
2
= 9.551, df = 2, N= 16, P= 0.008) and N. umbratica (Kruskal-
Wallis test, χ
2
=1.303,df=2,N=19,P=0.521)
Tab l e 4 Results of bivariate MCMCglmm testing for between-
individual and phenotypic correlations of aggressiveness and initial ac-
tivity in a novel environment in the three species
Species Between-
individual
correlation
Phenotypic
correlation
L. sclopetarius 0.190 0.112
Z. x-notata −0.080 0.024
N. umbratica 0.285 0.145
We compared constrained models (co-variances between and within in-
dividuals are constrained to zero; Covind0y;ind0z=0,Cove0y;e0z=0)and
unconstrained models (Cove0y;e0z= 0) and assumed significant correlation
when DIC unconstrained −DIC constrained <5. All correlations were
insignificant. DIC of unconstrained model was slightly smaller
(L. sclopetarius:ΔDIC = 0.64; N. umbratica: ΔDIC = 1.19). Detailed
results are given in Supplement 3
125 Page 10 of 15 Behav Ecol Sociobiol (2017) 71:125

environments. Our results are consistent with this idea, as
L. sclopetarius, our focal urban species, was also the most
active in our novel environment. Such increased activity in a
novel environment, or potential boldness, may also bring as-
sociated costs, i.e., when animals are overly active in the pres-
ence of a predator or other threats (Wilson 1998; Sih et al.
2003). For L. sclopetarius, however, boldness may bear little
cost related to predator exposure. Natural predators and re-
sponses to predation risk have not been assessed in these spe-
cies or populations, but it has been suggested previously that
L. sclopetarius have few natural predators (Kleinteich 2010).
Regardless, additional studies are required to test the potential
costs associated with increased activity in L. sclopetarius.
Contrary to our expectations, Z. x-notata exhibited the highest
levels of within-species aggressiveness followed by
L. sclopetarius and then N. umbratica. Our initial expectation
was that the most urban species, and that with the highest popu-
lation densities (L. sclopetarius), would be the most tolerant, or
exhibit the lowest levels of aggression. While aggressiveness
may generally be beneficial in territorial disputes, overt aggres-
siveness may be costly in high density populations due to high
incidences of injury and low survival rate (Holway 1998; Kralj-
Fišer and Schneider 2012). This potential cost of aggressiveness
may help explain observed differences in population density be-
tween L. sclopetarius and Z. x-notata.Zygiella x-notata can in-
deed be found in large aggregations in the field (Leborgne and
Pasquet 1987), but they always exhibit a lower density of indi-
viduals as compared to aggregations of L. sclopetarius
(Leborgne and Pasquet 1987; Schmitt and Nioduschewski
2007a,2007b). A higher level of aggressiveness in Z. x-notata
may help explain these differences in density. Following this line
of reasoning, we would expect N. umbratica, the most solitary
species, to exhibit high levels of aggression. In contrast, we found
N. umbratica to be inherently non-aggressive and to avoid con-
specifics. Based upon these results, we propose that their ob-
served isolation in nature is due, at least in part, to their web
structureand not theirlevel of aggression.Nuctenea spidersbuild
relatively large orb webs that catch sizeable prey (Bucher and
Entling 2011), and such webs likely require more structured hab-
itat. Previous studies support this idea, as increased densities of
N. umbratica individuals, in combination with lack of space, led
to individuals in poor body condition (Bucher and Entling 2011).
Ultimately,while aggressiveness level didnot exactly conformto
ourpredictionsof urban invasion,ourdata do suggestthat levelof
within-species aggressiveness might play a role in determining
population density once an environment is colonized for some
species while others might be constrained by habitat structure.
Beyondaverage behaviorlevels across species,previous stud-
ies have emphasized the importance of between-individual var-
iation in behavior for successful exploitation of urban environ-
ments (Møller 2010;Carrete and Tella2011; Bókony et al. 2012).
For example, Møller (2008) found that bird species that initially
colonized urban areas had more variable behavior than those that
failed in such colonization. Along similar lines, Fogarty et al.
(2011) suggested that different behavioral types are favored dur-
ing invasion process, e.g., bold and aggressive individuals are
good initial dispersers, whereas shy and socially tolerant individ-
ualsmay cause subsequentpopulationproliferation (e.g.,Clobert
et al. 2009;Coteetal.2010). In at least partial agreement with
these studies, we observed species-level differences in activity
level (highest in the urban species L. sclopetarius) simultaneous
with significant between-individual variation in activity and
within-sex aggressiveness in all three tested species. We propose
that the higher activity level of L. sclopetarius might have en-
abled their initial colonization of urban areas, as compared to the
other two species. Subsequently, as new individuals immigrated
and the population grew, variation among individuals in activity
and aggression may have facilitated increases in population den-
sity in L. sclopetarius. The individual differences were stable
over time with the repeatability estimates ranging from 0.43 to
0.49 for activity in a novel environment, and from 0.78 to 0.83 for
aggressiveness, which is concordant with results from compara-
ble invertebrate and vertebrate studies (Kralj-Fišer et al. 2007,
2012; Pruitt et al. 2008;Belletal.2009).
In comparison to repeatability estimates for aggressiveness,
spiders of all three species exhibited considerably lower (but still
significant) repeatability in activity when introduced to a novel
environment. This comparably lower repeatability estimate is
mainly due to higher within-individual variation, namely, higher
average plasticity. The pattern of change in activity to a novel
environment across two exposures also differed across species.
While L. sclopetarius prolonged the activity in the second trial,
Z. x-notata and N. umbratica shortened their activity durations. It
is possible that L. sclopetarius were desensitized/habituated due
to repeated trials, whereas Z. x-notata and N. umbratica re-
sponses might reflect sensitization. Alternatively, the species
may differ in their risk assessment of the new environment—
e.g., given that no predator were encountered, L. sclopetarius
may have estimated the environment to be safe, while Z. x-notata
and N. umbratica may require additional information before
attaining the same risk estimate. Other explanations exist, but it
seems likely that regardless of the underlying reason for the be-
havioral change, the altered responses likely result from learning
(Barron et al. 2015). Within species, we observed additional var-
iationas individual spiders didnotresponduniformly but differed
in degrees of behavioral change across the two repeated trials. In
contrast to our prediction that estimates of between-individual
variance in reaction norm slopes should be higher in the strictly
urban L. sclopetarius compared to Z. x-notata and N. umbratica,
we found that the three species exhibited comparable levels of
individual variation in behavioral plasticity. One potential inter-
pretationof these resultsisthat(variation in) behavioralchangein
reaction to novel vs. familiar stimuli may be adaptive in both city
exploiters as well as in suburban species.
The estimates of between-individual variance were remark-
ably high for aggressiveness in all three species, implying that
Behav Ecol Sociobiol (2017) 71:125 Page 11 of 15 125

different aggressiveness types are present in urban and subur-
ban species, regardless of whether they occur in high den-
sity aggregations or not. Our results from Bhigh density
experiments^support the hypothesis that consistent
between-individual variation in aggressiveness enhances
survival in high density groups. As in L. sclopetarius
(Kralj-Fišer and Schneider 2012), groups of Z. x-notata
consisting of both aggressive and tolerant spiders had
higher survival rates over 3 weeks than the groups com-
posed of either aggressive or tolerant individuals.
However, in N. umbratica—the species for which individ-
uals typically occur in isolation—survival rates were very
high and did not differ among groups of different aggres-
siveness type compositions. Additionally, in contrast to an
earlier study that documented a decrease in body condi-
tion with increased density in N. umbratica (Bucher and
Entling 2011), we observed increased body mass after
3 weeks. Perhaps, a longer exposure to high density con-
ditions would give more informative results.
The results for A. x-notata are consistent with the suggestion
that urban environments favor populations that consist of indi-
viduals exhibiting diverse, but stable, aggressiveness types,
which may facilitate high density aggregations. Variation in
behavioral types within the groups, in particular in social ani-
mals, has been repeatedly shown to enhance group fitness, e.g.,
through better survival and/or increased reproductive success
(Watters and Sih 2005; Jones et al. 2010;PruittandRiechert
2011), increased group productivity (Modlmeier and Foitzik
2011; Modlmeier et al. 2012), or task proficiency (Wright
et al. 2014; Laskowski et al. 2016). Various mechanisms have
been proposed to explain why diverse groups outperform
monotypic groups (Wolf and Weissing 2012; Montiglio et al.
2013). In orb-web spiders, individuals of different aggressive-
ness types may vary in their distribution within habitats
resulting in non-random interactions among behavioral types,
reduced competition among individuals, and consequently
more diverse habitat use (e.g. Kobler et al. 2009). In our exper-
iments in Z. x-notata, for example, in the Baggressive groups,^
most individuals might compete for the prime sites (frame cor-
ners), whereas in the mixed groups, tolerant individuals might
leave these sites to the aggressive ones and settle elsewhere.
While the aggressive groups suffered high mortality rates due
to intense antagonistic interactions, aggressive individuals were
far enough from each other to reduce competition in the mixed
group. In the Btolerant group,^survival rates resembled those in
Baggressive groups,^yet individuals gained body mass in the
former and decreased it in the latter. This suggests that, at least
in the laboratory conditions, groups of tolerant individuals do
better than groups of aggressive individuals. Additional field
experiments are needed to investigate the mechanisms allowing
mixed aggressive type groups to outperform groups of tolerant
or aggressive individuals only, perhaps related to functional
complementary or niche partitioning.
Finally, we failed to find significant correlations between
activity in a novel environment and aggressiveness, implying
that the two behavioral traits can vary independently in all
three species. Several studies comparing rural and urban pop-
ulations have found behavioral correlations in rural, but not in
urban, conspecific populations (Evans et al. 2010; Scales et al.
2011; Miranda et al. 2013); however, we found no behavioral
associations in either urban or suburban spiders. This suggests
that the association between behavioral traits is more flexible
in (sub)urban than rural environments. In other words, urban-
ization may lead to breakdown of behavioral syndromes,
which probably occurs through behavioral plasticity (Bell
and Sih 2007; Dingemanse et al. 2007;Bengstonetal.2014;
Royauté et al. 2015).
Conclusions
Prior and current evidence suggests that the ultimate city exploit-
er among orb-web spiders, L. sclopetarius,isabold,active,and
moderately aggressive species with high developmental plastic-
ity, a short life cycle, and high reproductive output (Mayntz et al.
2003; Kleinteich and Schneider 2011;Kralj-Fišer et al. 2014). In
comparison, the synanthropic species, Z. x-notata, exhibits high
aggressiveness, but lower levels of boldness and less plastic de-
velopment (Mayntz et al. 2003). Finally, the suburban
N. umbratica is non-aggressive and relatively inactive in novel
environments, with a rather canalized development and longer
life cycle (Kralj-Fišer et al. 2014). Despite these differences, the
three species exhibit similar levels of variation in behavioral traits
both between and within individuals. In the urban and suburban
species, the between-individual differences in aggressiveness
appeared highly repeatable, indicating that variation in aggres-
siveness types likely enables survival in high density conditions.
We found the evidence for both consistent individual differences
and plasticity in individuals’response to a novel environment,
suggesting that some degree of flexibility in reaction to novelty
may be crucial when adapting to urbanized environment. We
conclude that urban populations exhibit a complex pattern of
behavioral flexibility and behavioral stability, and that their rela-
tive roles may depend on the function of any given behavior.
Acknowledgements We thank Jutta Schneider for sharing her ideas
and for commenting on several versions of this manuscript; Chen-Pan
Liao for his advice in R; Tomma Dirks, Angelika Tabel-Hellwig, Rebeka
Šiling, and Klavdija Šuen for spider husbandry; and Klemen Čandek and
MatjažGregoričfor help with field work. SKF was granted a Humboldt
Postdoctoral Fellowship and a Humboldt Return Fellowship, and was
supported by the Slovenian Research Agency (grant Z1―4194). MK
was supported by the Slovenian Research Agency (grants P1-10236
and J1-6729).
All data analyzed during this study are included in this published
article and its supplementary information file 4.
125 Page 12 of 15 Behav Ecol Sociobiol (2017) 71:125

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