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Abstract

Urbanization poses serious extinction risks, yet some species thrive in urban environments. This may be due to a pronounced developmental plasticity in these taxa, since phenotypically, plastic organisms may better adjust to unpredictable urban food resources. We studied phenotypic plasticity in Nuctenea umbratica, a common European forest and urban vegetation spider. We subjected spiderlings to low (LF), medium (MF) and high (HF) food treatments and documented their growth and developmental trajectories into adulthood. Spiders from the three treatments had comparable numbers of instars and growth ratios, but differed in developmental periods. Longest developing LF spiders (♀ = 390, ♂ = 320 days) had the smallest adults, but MF (♀ = 300, ♂ = 240 days) and HF (♀ = 240, ♂ = 210 days) spiders reached comparable adult sizes through shorter development. While males and females had comparable instar numbers, females had longer development, higher growth ratios, adult sizes and mass; and while males adjusted their moulting to food availability, female moulting depended on specific mass, not food treatment. We discussed the patterns of Nuctenea sex-specific development and compared our results with published data on two other Holarctic urban colonizers (Larinioides sclopetarius, Zygiella x-notata) exhibiting high plasticity and fast generation turn-over. We conclude that despite relatively unconstrained developmental time in the laboratory enabling Nuctenea to achieve maximal mass and size-main female fitness proxies-their relatively fixed growth ratio and long generation turn-over may explain their lower success in urban environments.
ORIGINAL PAPER
Development and growth in synanthropic species:
plasticity and constraints
Simona Kralj-Fišer & Tatjana Čelik & TjašaLokovšek &
Klavdija Šuen & Rebeka Šiling & Matjaž Kuntner
Received: 2 April 2014 /Revised: 25 May 2014 /Accepted: 26 May 2014
#
Springer-Verlag Berlin Heidelberg 2014
Abstract Urbanization poses serious extinction risks, yet
some species thrive in urban environments. This may be due
to a pronounced developmental plasticity in these taxa, since
phenotypically, plastic organisms may better adjust to unpre-
dictable urban food resources. We studied phenotypic plastic-
ity in Nuctenea umbratica, a common European forest and
urban vegetation spider. We subjected spiderlings to low (LF),
medium (MF) and high (HF) food treatments and documented
their growth and developmental trajectories into adulthood.
Spiders from the three treatments had comparable numbers of
instars and growth ratios, but differed in developmental pe-
riods. Longest developing LF spiders (=390, =320 days)
had the smallest adults, but MF (=300, =240 days) and
HF (=240, =210 days) spiders reached comparable adult
sizes through shorter development. While males and females
had comparable instar numbers, females had longer develop-
ment, higher growth ratios, adult sizes and mass; and while
males adjusted their moulting to food availability, female
moulting depended on specific mass, not food treatment. We
discussed the patterns of Nuctenea sex-specific development
and compared our results with published data on two other
Holarctic urban colonizers (Larinioides sclopetarius, Zygiella
x-notata) exhibiting high plasticity and fast generation turn-
over. We conclude that despite relatively unconstrained devel-
opmental time in the laboratory enabling Nuctenea to achieve
maximal mass and sizemain female fitness proxiestheir
relatively fixed growth ratio and long generation turn-over
may explain their lower success in urban environments.
Keywords Arthropod development
.
Growth patterns
.
Life
history
.
Nuctenea umbratica
.
Spider
.
Urban ecology
Introduction
Among human-induced environmental changes, urbanization
currently represents one of the major threats to Earthsbiodi-
versity. Urbanization causes loss or fragmentation of native
habitats, modifications in community structures, pollution,
and c hanges in sensory environmen ts (McKinney 2002,
2008). In urban environments, food resources become spatial-
ly concentrated and their temporal availability oscillates more
arbitrarily (Shochat et al. 2006; Sol et al. 2013). While human-
induced changes imperil most taxa and place their populations
at risk of extinction, some organisms thrive in urban environ-
ments, proliferating and expanding their ranges (McKinney
2002, 2008). This raises the question of what mechanisms
enable them to tolerate urban environmental alterations.
Communicated by: Sven Thatje
S. Kralj-Fišer (*)
:
T. Čelik
:
T. Lokovšek
:
M. Kuntner
Institute of Biology, Scientific Research Centre, Slovenian Academy
of Sciences and Arts, Novi trg 2, P. O. Box 306, SI-1001 Ljubljana,
Slovenia
e-mail: simonakf@gmail.com
S. Kralj-Fišer
Faculty of Mathematics, Natural Sciences and Information
Technologies, University of Primorska, Glagoljaška 8,
SI-6000 Koper, Slovenia
K. Šuen
Biotechnical faculty, University of Ljubljana, Jamnikarjeva 101,
SI-1000 Ljubljana, Slovenia
R. Šiling
Institute for Water of the Republic of Slovenia, Hajdrihova 28 c,
SI-1000 Ljubljana, Slovenia
M. Kuntner
Department of Entomology, National Museum of Natural History,
Smithsonian Institution, NHB-105, PO Box 37012, Washington,
DC 20013-7012, USA
M. Kuntner
Centre for Behavioural Ecology & Evolution, College of Life
Sciences, Hubei University, Wuhan 430062, Hubei, China
Naturwissenschaften
DOI 10.1007/s00114-014-1194-y
Phenotypic plasticity, the ability of an organism to change a
phenotype in response to variation in the environment (West-
Eberhard 2003), may be a salient quality of those species that
thrive in cities (Sol 2003; Yeh and Price 2004). The important
components of phenotypic plasticity are adjustable life history
traits, such as developmental and growth patterns, size and age
at maturation, reproductive investment, and longevity (Stearns
1992;Roff2002). Organisms t hat are able to adjust life
histories to rapid environmental changes are expected to fare
better in urban environments than individuals with more can-
alized life history trajectories (e.g. Buczkowski 2010;
Kleinteich and Schneider 2011). In the latter, developmental
traits show low ability for phenotypic changes in response to
environmental conditions. However, both plasticity and cana-
lization have fitness costs and benefits (Van Buskirk and
Steiner 2009;Dmitriew2011).
Developmental and growth patterns determine age and size
at maturity, which significantly affect fitness (Stearns 1992;
Roff 2002). For instance, the growth rate and developmental
times affect vulnerability to predators exposure (Gotthard
2000) and determine a populations generation time. In most
arthropods, female adult massstrongly correlated with fe-
cundity (Suter 1990;Higgins1992;Head1995)affects the
net reproductive rate, R (mean number of female offspring a
mother produces during her lifetime) whereas in males, size at
maturity strongly relates to competitive abilities in malemale
contests and female choice (Christenson and Goist 1979;
Vo llra t h 1980;Andersson1994). Finally, the net reproductive
rate and generation time strongly relate to intrinsic rate of
population, r (i.e. per capita rate of population increase).
In arthropods, the exoskele ton grows in discrete steps
through mou lting, whereas mass ch anges continu ously
(Foelix 2010). According to Dyarsrule(Dyar1890), arthro-
pods exhibit a determined (also canalized) growth r ate
quantified as the ratio of two consecutive i nstar sizes
(Przibram and Megušar 1912;Cole1980) and are often con-
sidered to have a constant number of instars (Esperk et al.
2007). Growth plasticity, on the other hand, refers to variation
in growth rates in response to variation in environmental
conditions. A number of studies in arthropods have investi-
gated the effects of environmental conditions on variation in
developmental trajectories and growth rate (e.g. Gimnig et al.
2002
;Gillesetal.2010; Kleinteich and Schneider 2011), in
particular, in response to different temperature regimes (e.g. Li
and Jackson 1996; Robinson and Partridge 2001; Flenner
et al. 2010). In insects, studies of growth and developmental
plasticity depending on diet regimes have yielded mixed
results. While in some taxa exhibiting fixed instar numbers
Dyars rule receives support (e.g. Acrida exaltata, Ahmad
2012; Dendroctonus valens, Liu et al. 2014), other taxa show
significant plasticity in growth rates and developmental tra-
jectories depending on food supply (Atkinson and Sibly 1997;
Esperk et al. 2007).
Detailed studies revealed considerable species differences
in degrees of plasticity among developmental parameters, and
various parameters are often interdependent (e.g. Davidowitz
and Nijhout 2004). Higgins and Rankin (1996) described
eight possible combinations of canalized and plastic develop-
mental and growth parameters in arthropods resulting in var-
ious outcomes regarding age and size at maturity. Four of
these combinations (canalized inter-moult duration, canalized
instar number, canalized growth rate and fully plastic devel-
opmental pattern) were documented in empirical field re-
search (Higgins and Rankin 1996). For instance, the
hawkmoth, Manduca sexta, exhibits canalized maximum
inter-moult duration, but plasticity in instar number, growth
rate and pre-moult mass in response to diet (Nijhout and
Willams 1974;Nijhout1975; Safranek and Williams 1984).
The well-fed individuals might develop at higher growth rates
and might be able to reach critical mass for pupation and
metamorphosis through fewer instars (Kingsolver 2007). On
the other hand, poor nutrition in M. sexta might lead to
moulting after certain critical number of days even in the
absence of mass gain. In the milkweed bug, Oncopeltus
fasciatus, the number of instars is fixed, but the inter-moult
duration and growth rates are plastic (Nijhout 1979), and thus,
well-fed individuals develop earlier and at a higher mass.
Substantial difference in male and female body size is often
attributed to sex-specific selection, e.g. scramble competition
and malemale competition in males, and fecundity selection
in females (Andersson 1994;Head1995; Blanckenhorn 2005;
Blanckenhorn et al. 2007). At proximate level, size dimorphic
species exhibit sex-specific differences in growth and devel-
opment and also sex variation in plasticity in response to
environmental variation (reviewed in Stillwell et al. 2010).
For example, in M. sexta, males and females differ in plasticity
in the parameters critical for adult body size, i.e. growth rate
and critical mass for metamorphosis, in response to diet and
temperature (Stillwell and Davidowitz 2010).
Little is known about growth and developmental plasticity
in spiders, a species rich and ecologically important inverte-
brate clade-important terrestrial predators of insects and
known for some spectacular cases of female-biased sexual
size dimorphism (e.g. Kuntner et al. 2012). In spiders, growth
and development are believed to largely depend on food
availability (Miyashita 19 68). Cursori al spiders actively
search for food sources and seem to mostly exhibit plastic
growth and development patterns (e.g. Miyashita 1968;
Enders 1976; Li and Jackson 1997). On the other hand, orb-
web spiders are sit-and-wait predators whose ability to
behaviourally adjust to prey availability is limited to changing
web site, web position, and web properties (Herberstein and
Elgar 1994; Heiling and Herberstein 1998;Blackledgeetal.
2011). While this may suggest that they should be even more
adapted to temporal variations in foraging opportunities, the
results from empirical studies show ranges of growth and
Naturwissenschaften
developmental plasticity in orb weavers. For example, the
bridge spider (Larinioides sclopetarius) exhibits extreme plas-
ticity depending on food availability and fluctuation in virtu-
ally all life history traits (Kleinteich and Schneider 2011), and
comparable plasticity was reported i n Zygiella x-notata
(Mayntz et al. 2003), another synanthropic orb weaver. On
the other hand, while the neotropical Nephila clavipes shows
constant growth per ecdysis and pre-moult mass, its number of
moults and inter-moult duration are plastic (Higgins 1992,
1993; Higgins and Rankin 1996). Since only a handful of
species have been investigated, it is premature to attribute
synanthropic life styles to different degrees of phenotypic
plasticity, although the conjecture is logical. Developmental
and growth plasticity may have important ecological conse-
quences and may significantly predict success of species in
urban environments with buffered seasonality (and thus
prolonged food availability), but often spatially and temporal-
ly unpredictable food resources (Shochat et al. 2006;Kearney
et al. 2010).
To investigate these issues more closely, we asked if
growth and developmental plasticity depending on food avail-
ability differ between three orb-web spiders that vary in their
success as urban colonizers. We studied Nuctenea umbratica
and compared our results with the published data on two other
urban dwellers, L .sclopetarius (Kleinteich and Schneider
2011)andZ. x-notata (Mayntz et al. 2003). All three species
are orb-weaving spiders whose females may be found year
round in European urban areas but whose abundances vary.
The synanthropic L. sclopetarius and Z. x-notata are success-
ful colonizers of cities throughout the Holartic, their preferred
web sites are bridges, buildings, and other constructions. Their
success in the urban environment has been hypothesised to be
a consequence of their ability to adjust growth and develop-
ment to temporal fluctuations of prey (Mayntz et al. 2003;
Kleinteich and Schneider 2011). On the other hand, the study
species, Nuctenea umbratica is a ubiquitous European forest
dweller that also lives synanthropically, but in highly urban-
ized areas is either outcompeted by L. sclopetarius and Z. x-
notata, or is confined to habitat patches with low population
densities; in cities, they occupy trees and hedgerows in areas
without artific ial light (own data). We hypothesized that
Nuctenea is poorly pre-adapted for urban habitats due to lower
levels of growth and developmental plasticity (hence, more
canalized) compared with Larinioides and Zygiella.
Materials and methods
Study object
The walnut orb weaver, Nuctenea umbratica, is a common
Central European spider. These sizable spiders disperse by
ballooning in juvenile stage and prefer landscapes with semi-
open habitats, such as forest edges, hedgerows, orchards and
single trees (Bucher et al. 2010). While adult phenology peaks
between June and October, females can be found year long
(Nentwig et al. 2014). During the day, the spider hides under
cracks in the bark of trees or fences with a signal line con-
nected to its orb web, but assume a night foraging pose at web
hub. We collected subadult spiders from their webs on trees
and hedgerows along the Ljubljanica riverbank in Ljubljana,
Slovenia, between May and July 2010.
Rearing conditions
Spiderlings used in laboratory assays originated from 41
females that had been raised to adulthood and had mated
(one virgin male+one virgin female). We kept the egg sacs
at room temperature and sprayed them with water three times
a week. From 10 to 15 days after hatching, spiderlings were
separated and placed into 250-ml plastic cups, then randomly
subjected to three feeding regimes: low food (LF; N=57),
medium food (MF; N=45) and high food (HF; N=64). The
spiderlings in LF received one Drosophila fly once a week,
those in MF one fly twice a week and those in HF two flies
twice a week. After the fifth moult, we offered juvenile spiders
the same number of prey as above, but substituted fruit flies
for blowflies (Calliphora sp.) to secure their increased nutri-
tional requirements. We checked each spider five times a week
for moulting following their second moult (first moulting
occurs in the egg sac about 3 days after hatching). Any spider
that had moulted was weighed using an electronic balance to
an accuracy of 0.001 g. From December 2011 to June 2013 we
monitored the development of 166 individuals. Of these, 81
spiders reached adulthood (N=49, N=32; HF=33, MF=
27, LF=21), 34 died and 51 were lost. At maturity, we fixed
the spiders in 70 % ethanol and microscopically measured the
length of their first patella+tibia and the carapace width.
Developmental and growth parameters
We documented the following parameters for each individual:
number of instars, developmental time (time from hatching to
adulthood), mean inter-moult duration, mean growth ratio,as
well as mass and size at maturity. The proxy for size at
maturity was the length of the first patella+tibia (Higgins
et al. 2011). The growth ratio of an individual from previous
instar (n
i-1
) into current instar (n
i
) was defined as the mass of n
i
divided by the mass of n
i-1
(e.g. Kleinteich and Schneider
2011).
Statistical analyses
Most of the data were not normally distributed, and were
therefore log transformed to meet the assumption of homoge-
neity of variances. We compared developmental parameters
Naturwissenschaften
between treatments, sexes and sex × treatment using General
Linear Model (GLM), and applied the Bonferroni post hoc
test. Although the adult mass data were normally distributed,
they violated the assumption of Levenestestofhomogeneity
of variances (p <0.05) despite various transformations.
Therefore, we here used two GLMs for sex and treatment
differences separately (Levenes tests of homogeneity of var-
iances were then non-significant); we used Bonferroni tests to
analyse differences between the three treatments. In the cases
where significant effects of the treatments and sex (develop-
mental time, mean inter-moult duration, mass and size at
maturity) were detected, we further tested differences between
treatments for males and females separately using GLMs; we
used Bonferroni or Games-Howell post hoc tests. Here, all
parameters met the assumption of Levenestestofhomoge-
neity of variances.
We examined the effect of treatments on masstrans-
formed with log (x+1)over development using repeated
measures ANOVA with Bonferroni post hoc test. We tested
the linear relationships between life-history trajectories for
males and females separately using Pearsons correlations.
The mortality and loss were compared between treatments
using a Pearsons χ
2
. All tests, performed in SPSS Statistics
20, were two-tailed, and significance was set at p<0.05.
Results
Treatment effects
Non-transformed data of growth and developmental parame-
ters in Nuctenea spiders from different food treatments are
given in Table 1. Spiders that received variable food quantities
during development did not significantly differ in the number
of instars until maturity and in the mean growth ratios
(Table 2). However, they significantly differed in the mean
inter-moult duration, total developmental time, adult patella+
tibia I length and carapace width, as well as in the mass at
maturity (Table 2). Spiders reared under HF matured earlier
than spiders from both MF and LF (p<0.001), and those from
MF matured earlier than spiders from LF (p <0.001).
Similarly, spiders from different treatments, on average, spent
variable periods in each instar; spiders from HF had shorter
inter-moult durations than MF and LF spiders, and MF spiders
had shorter inter-moult durations than LF spiders (HF:MF, p=
0.001; HF:LF, p<0.001; MF:LF, p<0.001). At adulthood, the
spiders from HF had the longest patella+tibia I, whereas those
from LF had the shortest legs (HF:MF, p=0.006; HF:LF,
p<0.001; MF:LF, p= 0.022). The latter also reached maturity
at significantly lower mass (HF:LF, p<0.001; MF:LF, p=
0.003) and developed narrower carapaces (HF:LF, p<0.001;
MF:LF, p<0.003). Spiders from HF and MF, however, did not
vary in either mass at maturity (p=0.698) nor in carapace
width (p=0.921).
Inter-sex differences
We found sex differences in all measured developmental
parameters, except i n the number of instars (Table 2;
Figs. 1b f). Females exhibited higher growth rati os
(p<0.001), spent more time in each instar (p<0.001) and
needed more time to reach adulthood (p<0.001) than did
males. Accordingly, adult females were heavier than males
(p<0.00 1) and developed wider carapaces (p<0.001) but
shorter patella+tibia I (p<0.001).
Intra-sex differences
The treatments somewhat differently affected males and fe-
males inter-moult durations and total developmental time:
females from the three treatments significantly differed in total
developmental time (Fig. 1c) and mean inter-moult durations
(LF:MF, p
=0.004; LF:HF, p <0.001; MF:HF, p =0.006).
Males from LF had the longest total developmental times
and inte r-moult durations (total developmental times,
Fig. 1c; inter-moult durations, LF:MF, p<0.001; LF:HF,
p<0.001); MF and HF males however had comparable devel-
opmental periods (total developmental times, Fig. 1c;inter-
moult durations, p=1). The adult size of both sexes was
smallest in LF spiders, however, MF and HF spiders were of
similar sizes (Fig. 1d, e). The mass at maturity differed be-
tween all treatments in males, but adult female mass differed
only between LF and HF (Fig. 1f).
Detailed analyses revealed that males from different food
supply treatments significantly varied in mass at moulting into
given instars (F
19,2
=4.744, p=0.021, Fig. 2b). While female
mass at specific moulting was independent of food supply
(F
41,2
=2.378, p=0.105; Fig. 2a), the males from HF moulted
at higher mass than males from LF and MF (LF:MF, p=1;
LF:HF, p=0.032; MF:HF, p=0.125; Fig. 2a, b).
Table 3 summarizes correlations between the developmen-
tal parameters. The mean inter-moult duration correlated pos-
itively with total developmental time and negatively to num-
berofinstars.Inbothsexes,thelowermeangrowthratio
related to a higher number of instars and longer development;
however, the latter relationship was significant only in fe-
males. In males, but not in females, the spiders with longer
inter-moult durations developed shorter legs and lower adult
body mass. The higher growth ratio related to longer legs and
wider carapaces in males.
Mortality and loss during the study
During the experiments, 20.48 % (N=34) of individuals died;
however, the occurrence of death was independent of the food
Naturwissenschaften
supply (Pearsons χ
2
=0.549, df=2,N=166, p=0.743). Avery
high percentage, 30.72 %, of spiders were lost during exper-
iments (N=51). Significantly more spiders escaped/were lost
from LF than from MF and HF (Pearsons χ
2
=6.021, df=2,
N=166, p=0.049), which appears to be a consequence of
longer periods of small spiderling sizes.
Discussion
The results of our study suggest that the partially synanthropic
spider Nuctenea umbratica exhibits a canalized growth rate;
growth ratios of individuals reared under different food quan-
tity did not significantly vary. The spiders developed through
Table 2 The effects of treatments
(high, medium and low food sup-
ply), sex, and treatment×sex on
developmental parameters. Sig-
nificant relationships are in italics
Developmental parameter Independent factors F Significance
Number of instars Treatment 0.404 0.669
Sex 2.439 0.123
Treatment×sex 0.800 0.453
Mean growth ratio Treatment 2.121 0.127
Sex 198.439 <0.001
Treatment×sex 0.165 0.848
Mean inter-moult duration (days) Treatment 42.234 <0.001
Sex 47.447 <0.001
Treatment×sex 1.002 0.372
Total developmental time (days) Treatment 73.443 <0.001
Sex 30.038 <0.001
Treatment×sex 1.513 0.227
Length patella+tibia I (mm) Treatment 18.691 <0.001
Sex 51.038 <0.001
Treatment×sex 0.031 0.969
Carapace width (mm) Treatment 29.54 <0.001
Sex 67.734 <0.001
Treatment×sex 2.044 0.138
Mass at maturity (g) Treatment 11.146 <0.001
Sex 92.398 <0.001
Table 1 Median (first, third quartile) values of non-transformed parameters in spiders from low (LF), medium (MF) and high food (HF) treatment
during development
Parameter Sex Treatment
LF MF HF
Number of instars 8 (7, 8.25) 7 (7, 8) 7 (7, 8)
7 (6,8) 7 (6, 8) 7 (6.5, 8)
Mean inter-moult duration (days) 63.88 (58.18, 72.75) 48.2 (42, 53.8) 38.4 (35.21, 43.94)
64.5 (54.8, 73.14) 39.33 (33.11, 45.4) 35.75 (30.77, 42.85)
Total developmental time (days) 390.5 (342.75, 466.25) 300 (282, 320) 237.5 (222.25, 261.5)
320 (307, 365) 239 (210.25, 257.25) 208 (193.5, 225)
Mean growth ratio 1.82 (1.72, 2.25) 2 (1.8, 2.4) 2.09 (1.97, 2.3)
1.77 (1.68, 1.92) 1.95 (1.91, 2.19) 2.14 (1.95, 2.58)
Mass at maturity (g) 0.09 (0.06, 0.1) 0.09 (0.09, 0.1) 0.11 (0.1, 0.12)
0.04 (0.04,0.05) 0.06 (0.05, 0.06) 0.07 (0.06, 0.07)
Length tibia+patella I (mm) 4.6 (4.15, 5.17) 5.18 (5.05, 5.58) 5.6 (5.52, 5.78)
5.33 (5.02, 5.64) 6.14 (5.82, 6.42) 6.49 (6.04, 6.73)
Carapace width (mm) 3.14 (2.73, 3.26) 3.82 (3.66, 4.01) 3.95 (3.72, 4.11)
2.75 (2.68, 2.88) 3.09 (2.93, 3.18) 3.28 (3.03, 3.41)
Naturwissenschaften
variable number of instars (i.e. 69; Fig. 1a) independently of
sex and food availability. However, individuals from
different feeding regimes needed different periods of
time to reach adulthood, with more food availability
corresponding to earlier maturation. While adult sizes
of spiders from medium and high food treatments ex-
hibited comparable sizes, the spiders from low food
treatment were the smallest.
MalesFemales
log (carapace width) [mm]
.60
.55
.50
.45
.40
____________________
________
_________
______________
*
*
*
*
_______________________________________________________
*
MalesFemales
log (total developmental time) [days]
2.7
2.6
2.5
2.4
2.3
_________
________
_________
______________
*
*
*
*
_______________________________________________________
*
___________________
*
MalesFemales
log (patella + tibia I lenght) [mm]
.85
.80
.75
.70
.65
.60
____________________
________
_________
______________
*
*
*
*
_______________________________________________________
*
MalesFemales
adult mass [mg]
.12
.10
.08
.06
.04
.02
____________________
_________
______________
*
*
*
_______________________________________________________
*
________
*
MalesFemales
log (mean growth ratio)
.55
.50
.45
.40
.35
.30
.25
__________________________________________________
*
MalesFemales
log (number of moults)
.92
.90
.88
.86
.84
.82
(a) (b)
(c) (d)
(e) (f)
LEGEND - Food supply during development:
low (LF)
medium (MF)
high (HF)
Fig. 1 Growth and
developmental parameters of
spiders subjected to low food
(LF), medium food (MF) and
high food (HF) supply during
development. Error bars means±
SE of a number of instars; b mean
growth ratios; c total
developmental time (: p
(LF:MF)
=
0.005, p
(LF:HF)
<0.001, p
(MF:HF)
<
0.001; : p
(LF:MF)
<0.001,
p
(LF:HF)
<0.001, p
(MF:HF)
=0.692)
d adult patella+tibia I length (:
p
(LF:MF)
=0.018, p
(LF:HF)
<0.001,
p
(MF:HF)
=0.097; : p
(LF:MF)
=
0.018, p
(LF:HF)
<0.001, p
(MF:HF)
=
0.303); e adult carapace width (:
p
(LF:MF)
<0.001, p
(LF:HF)
<0.001,
p
(MF:HF)
=1; : p
(LF:MF)
=0.002,
p
(LF:HF)
<0.001, p
(MF:HF)
=0.223);
and f mass at maturity (:
p
(LF:MF)
=0.305, p
(LF:HF)
=0.04,
p
(MF:HF)
=0.061; : p
(LF:MF)
<
0.001, p
(LF:HF)
<0.001, p
(MF:HF)
=
0.037). Asterisk indicates
significant differences (p<0.05)
Naturwissenschaften
We found no significant variation in average growth ratios
between spiders from the three different food treatments;
however, MF and HF spiders matured at larger sizes than LF
spiders. This seemingly contradictory data may result from
individual differences and/or inter-relatedness between
growth rate and number of instars. To examine the former
explanation, we would have to test genetically related spiders
originating from the same mother. The results on the
individual level (correlations) may be insightful: growth rate
negatively correlated to instar numbers (the latter was inde-
pendent of food supply, but highly variable; Fig. 1a). The
above relationships suggest that an individual with, e.g. low
growth rate could add moult(s), which may result in a body
size comparable to individuals with relatively higher growth
rates but lower number of instars. Furthermore, females may
invest more nutrients into eggs than into measured body size
proxies (carapace width and first leg length). This may explain
why LF females had smaller size proxies but a comparable
mass to MF females. Such growth and developmental patterns
are likely a daptiv e, becau se in fe males mass relat es to
fecundity.
Developmental plasticity and exploitation of urban habitats
We contrast our results with those o n Larinioides and
Zygiella, two spiders that typically abound in highly urbanized
areas and that show higher levels of growth and developmen-
tal plasticity (Mayntz et al. 2003; Kleinteich and Schneider
2011). Larinioides (L. sclopetarius)andZygiella (Z. x-notata)
decrease or increase numbers of instars and adjust growth
ratio to food availability, and may also mature at significantly
variable ages, sizes and mass (Mayntz et al. 2003;Kleinteich
and Schneider 2011). While developmental rate seems to be
plastic to some degree in Nuctenea as well, our prediction that
Nuctenea would show more canalized growth compared with
the two urbanites was met. The comparison between the three
spider species that vary in their success of inhabiting urban
areas lends support for our hypothesis that high growth and
developmental plasticity in response to food resources could
be a preadaptation to urban environments. We found no study
on invertebrates comparing urban and non-urban species/
populations growth and developmental plasticity; however,
data from several studies suggest that plasticity may be im-
portant for coping with human-altered environment; in in-
sects, plasticity in developmental trajectories depending on
food supply during juvenile stage has been found mainly in
economically important pests (reviewed in Esperk et al. 2007)
and in the dipteran Aedes aegypti, a vector of human patho-
gens including dengue and yellow fever (Couret et al. 2014).
Growth plasticity in response to diet has been shown in, e.g.
Manduca sexta, a pest feeding on solanaceous plants
(Kingsolver 2007).
Highly urbanized areas support unpredictably abundant
resources. Insects, as the most important spider prey, may
show high abundances near food wastes and may have
prolonged season of activity (e.g. Kearney et al. 2010), but
their numbers can fluctuate unpredictably. Insects are also
abundant near city lights. Artificially lit urban habitats are
commonly inhabited by Zygiella and Larinioides (Leborgne
and Pasquet 1987; Heiling and Herberstein 1999;Kralj-Fišer
and Schneider 2012), but not Nuctenea (this study). Zygiella
Instar
87654321
log (weight +1) [mg]
.05
.04
.03
.02
.01
.00
F = 2.378
p = 0.105
Instar
98765432
log (weight +1) [mg]
.030
.025
.020
.015
.010
.005
.000
F = 4.744
p = 0.021
(a)
(b)
LEGEND
Food supply during development:
low (LF)
medium (MF)
high (HF)
Fig. 2 Mass over development measured shortly after moulting in given
instars. Error bars means±SE of mass in females (a)andmales(b)
Naturwissenschaften
response to increased prey availability is highly plastic: they
mature earlier and produce more and heavier eggs (Spiller
1992). They develop in cca. 160 days under unlimited food
accessibility (Mayntz et al. 2003), and might potentially have
two generations per year in favourable conditions. Larinioides
fed with high numbers of prey develop even faster, in approx-
imately 60 days (Kleinteich and Schneider 2011), and may
have up to four generations per year in laboratory conditions
(Schneider personal observation). Accelerated growth, earlier
maturation and reproduction under high prey abundance were
proposed to enable the bridge spider to successfully proliferate
in urban habitats (Kleinteich and Schneider 2011). In success-
ful urban spiders such as Zygiella and Larinioides,growthand
developmental plasticity likely facilitates and, in combination
with high food availability, results in shorter generation turn-
over (intrinsic rate of population) and increased fitness (net
reproductive rate), and consequently, in rapid population
growth.
In comparison with Zygiella and Larinioides, the develop-
ment of Nu ctenea is much slower and does not become
accelerated with abundant and constant food supply, with
artificially longer light periods, nor with increased winter
temperature (i.e. the laboratory conditions in our study). In
the laboratory conditions, well-fed spiderlings that had
hatched in November/December, matured only in July to
October (or in roughly 240 days in females; 210 days in
males; Table 1), which is not before their natural mating
season in the field (Nentwig et al. 2014). However, the deter-
mined growth ratio precluded timely development of spiders
with a highly restricted food supply (LF). Spiders from LF did
not exhibit higher mortality; however, females and males
needed, on average, 390 and 320 days, respectively, from
hatching to maturation and were relatively smaller as adults
(Table 1). We believe their long development and inferior size
would have severe fitness consequences in the field. Juvenile
females would miss the mating opportunities during the main
reproductive season from June to October. Even if they did
mate, their reproductive output, which in spiders generally
relates to body mass (Suter 1990;Higgins1992;Head1995),
would be reduced compared with well-fed females. Males
maturing late in reproductive season would also exhibit low
mating success as their small size would be disadvantageous
in malemale contests (Christenson and Goist 1979; Vollrath
1980; Foellmer and Fairbairn 2005). Therefore, we propose
that Nuctenea individuals may fail to survive and reproduce in
urban environments with low/sporadic prey availability . We
suggest that their canalized growth ratio and slow generation
turn-over (with up to one generation per year) precludes their
Table 3 Pearsons correlations between developmental parameters for females (in italics, above right) and males (in bold, below, left). Significant
relationships are underlined
DT NI ID GR MM PTL CW
DT r 0.139 0.786 0.317 0.111 0.279 0.068
P0.339
<0.001 0.027 0.448 0.070 0.663
N 494949494343
NI r 0.165 0.340 0.368 0.052 0.018 0.048
P 0.366
0.017 0.009 0.725 0.908 0.759
N 32 49 49 49 43 43
ID r 0.737 0.435 0.002 0.140 0.238 0.170
P
<0.001 0.013 0.988 0.337 0.124 0.276
N 32 32 49 49 43 43
GR r 0.289 0.481 0.016 0.149 0.073 0.029
P 0.108
0.005 0.932 0.308 0.643 0.854
N 32 32 32 49 43 43
MM r 0.526 0.222 0.550 0.227 0.872
P
0.002 0.223 0.001 0.212 <0.001
N 32 32 32 32 43
PTL r 0.520 0.030 0.473 0.415 0.595 0.631
P
0.009 0.988 0.020 0.044 0.002 <0.001
N 24 24 24 24 24 43
CW r 0.513 0.163 0.541 0.550 0.848 0.738
P
0.010 0.446 0.006 0.005 <0.001 <0.001
N 24 24 24 24 24 24
DT total developmental time, NI number of instars, ID mean inter-moult duration, GR mean growth ratio, MM mass at maturity, PTL adult patella+tibia I
length, CW adult carapace width
Naturwissenschaften
success in the stochastic urban environments where they face
competitors with greater developmental plasticity and faster
generation turn-over such as Larinioides and Zygiella.
While Nuctenea exhibited limited plasticity in the growth
ratio, their total developmental time highly depended on food
abundance. In HF treatment, spiders spent less time in an
instar and matured earlier than those f rom LF treatment.
Despite disadvantages described above, the MF spiders reach
adulthood at size and mass allowing them to optimize their
fitness in given environmental conditions. Females from re-
stricted food supply (MF) needed on average 300 days to
adulthood, and thus matured in the late reproductive season;
however, their body size and mass was not significantly lower
from HF females. Consequently, they might have fewer mat-
ing opportunities in the field, yet, when mated, their repro-
ductive output should be comparable with HF females, which
in our study, received double amounts of food. Therefore, it is
plausible to expect that females with adequate food supply
(MF) would be able to minimize their fitness consequences
compared with well-fed females. On the other hand, males
from MF matured over similar periods than HF males, how-
ever, at the smaller mass. Such sex variation in developmental
plasticity is likely adaptive; while males need to mature time-
ly, females need to increase their fecundity.
Intra-sex differences
Nuctenea spiders exhibited sex differences in growth and
developmental trajectories: males exhibited lower growth ra-
tios and shorter inter-moult durations, but matured earlier and
reached lower mass and narrower carapaces, but longer first
legs than females. These differences are in accordance with
other moderately sexually sized dimorphic spiders with
protandric mating system (e.g. Kralj-Fišer et al. 2013). Food
availability affected developm ental times in both sexes.
However, females moulted into a given instar at a specific
mass independently of the food treatment, whereas males
moulting pattern shifted to lower mass when food was restrict-
ed. These results suggest that males exhibit more plastic
development than females. Similarly, a study on the
Mediterranean tarantula (Lycosa tarantula)foundamore
canalized development to adult size in females than in males
(Fernández-Montraveta and Moya-Laraño 2007). Our data
suggest that femalesbut not maleshad rather fixed critical
mass to moult into the next instar and to reach maturity (cca.
0.06 g; Table 1, Fig. 1). This sex difference in plasticity is
logical since female adult mass strongly relates to fecundity,
affecting her fitness (Suter 1990;Higgins1992;Head1995).
Adult males, on the other hand, are more time-restricted; they
are usually not found during winter times in the field and such
adjustments likely enable them to catch up to the reproductive
season relatively independently of the mass and size at matu-
rity (when compared to females). Such data are in accordance
with scramble competition acting on males in female-biased
sexually size dimorphic species (Andersson 1994). Sex dif-
ferences in plasticity of mechanisms affecting body size in
response to diet have been also found in some sexually sized
dimorphic insects, e.g. the hawkmoth, Manduca sexta and
Australian fly, Te lostylinus angusticollis (Bonduriansky
2007) suggesting complex sex-specific responses to environ-
mental variation.
The restriction of food treatments was similar in the three
compared spider studies (Mayntz et al. 2003;Kleinteichand
Schneider 2011), except that in the HF treatment, Zygiella and
Larinioides received unlimited food (Mayn tz et al. 2003;
Kleinteich and Schneider 2011), but Nuctenea were restricted
to two flies twice a week. While this could have biased our HF
data, we find it unlikely because the growth rate and instar
number did not differ between LF and MF treatments, and
because females moulted into specific instars at similar masses
regardless of food conditions. Therefore, a rather canalized
growth rate and plastic inter-moult duration would also likely
be detected if the HF spiders were fed ad libitum.
Conclusions
Nuctenea umbratica exhibits elements of both canalization
and plasticity in growth and developmental trajectories. While
they are unconstrained in developmental time (in the labora-
tory) enabling them to achieve maximal mass and sizemain
fitness proxiesin give n condition s, the relati vely fixed
growth ratio and long generation turn-over may be the reasons
for their relatively lower success in the urban environments
when compared with urban achievers such as Zygiella and
Larinioides.InNuctenea, the increased terminal female sizes
affecting the net reproductive rate (R) likely counter-balance
the slow generation turn-over, leading to stable population
size. In Zygiella and Larinioides,increasedR and short gen-
eration time relate to a high intrinsic rate of population growth
in favourable conditions (Kingsolver and Huey 2008), and to
a high urban colonization success.
Acknowledgments This work was funded by the Slovenian Research
Agency (grants Z14194 and P10236).
References
Ahmad T (2012) On the food preferences and application of Dyars rule
to different hopper instars of Acrida exaltata Walker (Orthoptera:
Acrididae). Zool Ecol 22:114124
Andersson MB (1994) Sexual selection. Princeton University Press
Atkinson D, Sibly RM (1997) Why are organisms usually bigger in
colder environments? Making sense of a life history puzzle.
Trends Ecol Evol 12:235239
Naturwissenschaften
Blackledge TA, Kuntner M, Agnarsson I (2011) The form and function of
spider orb webs: evolution from silk to ecosystems. In: Casas J (ed)
Advances in Insect Physiology, vol 41. Academic Press, Burlington,
pp 175262
Blanckenhorn WU (2005) Behavioral causes and consequences of sexual
size dimorphism. Ethology 111:9771016
Blanckenhorn WU, Dixon AF, Fairbairn DJ, Foellmer MW, Gibert P, van
der Linde K, Wiklund C (2007) Proximate causes of Renschs rule:
does sexual size dimorphism in arthropods result from sex differ-
ences in development time? Am Nat 169:245257
Bonduriansky R (2007) The evolution of condition-dependent sexual
dimorphism. Am Nat 169:919
Bucher R, Herrmann JD, Schüepp C, Herzog F, Entling MH (2010)
Arthropod Colonisation of trees in fragmented landscapes depends
on species traits. Open Ecol J 3:111117
Buczkowski G (2010) Extreme life history plasticity and the evolution of
invasive characteristics in a native ant. Biol Invasions 12:33433349
Christenson TE, Goist KC (1979) Costs and benefits of malemale
competition in the orb weaving spider, Nephila clavipes. Behav
Ecol Sociobiol 5:8792
Cole BJ (1980) Growth ratios in holometabolous and hemimetabolous
insects. Ann Entomol Soc Am 73:489491
Couret J, Dotson E, Benedict MQ (2014) Temperature, larval diet, and
density effects on development rate and survival of Aedes aegypti
(Diptera: Culicidae). PLoS One 9:e87468
Davidowitz G, Nijhout HF (2004) The physiological basis of reaction
norms: the interaction among growth rate, the duration of growth
and body size. Integr Comp Biol 44:443449
Dmitriew CM (2011) The evolution of growth trajectories: what limits
growth rate? Biol Rev 86:97116
Dyar HG (1890) The number of molts of Lepidopterous Larvae. Psyche
5:420422
Enders F (1976 ) S ize, fo od-findin g, an d D yar's constant. Environ
Entomol 5:110
Esperk T, Tammaru T, Nylin S (2007) Intraspecific variability in number
of larval instars in insects. J Econ Entomol 100:627645
Fernández-Montraveta C, Moya-Laraño J (2007) Sex-specific plasticity
of growth and maturation size in a spider: implications for sexual
size dimorphism. J Evol Biol 20:16891699
Flenner I, Richter O, Suhling F (2010) Rising temperature and develop-
ment in dragonfly populations at different latitudes. Freshwater Biol
55:397410
Foelix R (2010) Biology of spiders. Oxford University Press
Foellmer MW, Fairbairn DJ (2005) Competing dwarf males: sexual
selection in an orb-weaving spider. J Evol Biol 18:629641
Gilles J, Lees R, Soliban S, Benedict M (2010) Density-dependent effects in
experimental larval populations of Anopheles arabiensis (Diptera:
Culicidae) Can Be Negative, Neutral, or Overcompensatory
Depending on Density and Diet Levels. J Med Entomol 49:10011011
Gimnig JE, Ombok M, Otieno S, Kaufman MG, Vulule JM et al (2002)
Density-dependent development of Anopheles gambiae (Diptera:
Culicidae) Larvae in Artificial Habitats. J Med Entomol 39:162172
Gotthard K (2000) Increased risk of predation as a cost of high growth
rate: an experimental test in a butterfly. J Anim Ecol 69:896902
Head G (1995) Selection on fecundity and variation in the degree of
sexual size dimorphism among spider species (Class Araneae).
Evolution 49:776781
Heiling AM, Herberstein ME (1998) The web of Nuctenea sclopetaria
(Araneae, Araneidae): relationship between body size and web
design. J Arachnol 26:9196
Heiling AM, Herberstein ME (1999) The importance of being larger:
intraspecific competition for prime web sites in orb-web spiders
(Araneae, Araneidae). Behaviour 136:669677
Herberstein ME, Elgar MA (1994) Foraging strategies of Eriophora
transmarina and Nephila plumipes (Araneae: Araneoidea):
Nocturnal and diurnal orb-weaving spiders. Aust J Ecol 19:451457
Higgins LE (1992) Developing plasticity and fecundity in the orb-
weaving spider Nephila clavipes. J Arachnol 20:94106
Higgins LE (1993) Constraints and plasticity in the development of
juvenile Nephila clavipes in Mexico. J Arachnol 21(10711):9
Higgins LE, Rankin MA (1996) Different pathways in arthropod
postembryonic development. Evolution 50:573582
Higgins LE, Coddington JA, Goodnight C, Kuntner M (2011) Testing
ecological and developmental hypotheses of mean and variation in
adult size in nephilid orb-weaving spiders. Evol Ecol 25:12891306
Kearney MR, Briscoe NJ, Karoly DJ, Porter WP, Norgate M, Sunnucks P
(2010) Early emergence in a butterfly causally linked to anthropo-
genic warming. Biol Lett 6:674677
Kingsolver JG (2007) Variation in growth and instar number in field and
laboratory Manduca sexta. Proc R Soc Lond Biol 274:977981
Kingsolver JG, Huey RB (2008) Size, temperature, and fitness: three
rules. Evol Ecol Res 10:251268
Kleinteich A, Schneider JM (2011) Developmental strategies in an inva-
sive spider: constraints and plasticity. Ecol Entomol 36:8293
Kralj-Fišer S, Schneider JM (2012) Individual behavioural consistency
and plasticity in an urban spider. Anim Behav 84:197204
Kralj-Fišer S, Gregorič M, Lokovšek T, Čelik T, Kuntner M (2013) A
glimpse into the sexual biology of the zygiellid spider genus
Leviellus. J Arachnol 41:387391
Kuntner M, Zhang S, Gregorič M, Li D (2012) Nephila female gigantism
attained through post-maturity molting. J Arachnol 40:344346
Leborgne R, Pasquet A (1987) Influences of aggregative behaviour on
space occupation in the spider Zygiella x-notata
(Clerck). Behav
Ecol Sociobiol 20:203208
Li D, Jackson RR (1996) How temperature affects development and
reproduction in spiders: a review. J Therm Biol 21:245274
Li D, Jackson RR (1997) Influence of diet on survivorship and growth in
Portia fi mbriat a, an araneophagic jumping spider (Araneae:
Salticidae). Can J Zool 75:16521658
Liu Z, Xu B, Sun J (2014) Instar numbers, development, flight period,
and fecundity of Dendroctonus valens (Coleoptera: Curculionidae:
Scolytinae) in China. Ann Entomol Soc Am 107:152157
Mayntz D, Toft S, Vollrath F (2003) Effects of prey quality and availabil-
ity on the life history of a trap-building predator. Oikos 101:631638
McKinney ML (2002) Urbanization, biodiversity, and conservation the
impacts of urbanization on native species are poorly studied, but
educating a highly urbanized human population about these impacts
can greatly improve species conservation in all ecosystems.
Bioscience 52:883890
McKinney ML (2008) Effects of urbanization on species richness: a
review of plants and animals. Urban Ecosyst 11:161176
Miyashita K (1968) Growth and development of Lycosa T-insignita Boes.
et Str. (Araneae: Lycosidae) under different feeding conditions. Appl
EntomolZool3:8188
Nentwig W, Blick T, Gloor D, Hänggi A, Kropf C (2014) Araneae,
spiders of Europe (v. 3). Available online at: http://www.araneae.
unibe.ch/
Nijhout HF (1975) A threshold size for metamorphosis in the tobacco
hornworm, Manduca sexta (L.). Biol Bull 149:214225
Nijhout HF (1979) Stretch-induced moulting in Oncopeltus fasciatus.J
Insect Physiol 25:277281
Nijhout HF, Willams CM (1974) Control of moulting and metamorphosis
in the tobacco hornworm, Manduca sexta (L.): cessation of juvenile
hormone secretion as a trigger for pupation. J Exp Biol 61:493501
Przibram H, Megušar F (1912) Wachstumsmessungen an Sphodromantis
bioculata Burm. Dev Genes Evol 34:680741
Robinson S, Partridge L (2001) Temperature and clinal variation in larval
growth efficiency in Drosophila melanogaster. J Evol Biol 14:14
21
Roff DA (2002) Life history evolution. Sinauer, Sunderland
Safranek L, Williams CM (1984) Critical weights for metamorphosis in
the tobacco hornworm, Manduca sexta. Biol Bull 167:555567
Naturwissenschaften
Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From
patterns to emerging processes in mechanistic urban ecology. Trends
Ecol Evol 21:186191
Sol D (2003) Behavioural flexibility: a neglected issue in the ecological
and evolutionary literature? In: Reader SM, Laland KN (eds)
Animal innovation. Oxford University Press, Oxford, pp 6382
Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments
for a life in the city. Anim Behav 85:11011112
Spiller DA (1992) Numerical response to prey abundance by Zygiella x-
notata (Araneae, Araneidae). J Arachnol 179188
Stearns SC (1992) The evolution of life histories. Oxford University
Press, London
Stillwell RC, Davidowitz G (2010) Sex differences in phenotypic plas-
ticity of a mechanism that controls body size: implications for sexual
size dimorphism. Proc R Soc Lond Biol 277:38193826
Stillwell RC, Blanckenhorn WU, Teder T, Davidowitz G, Fox CW (2010)
Sex differences in phenotypic plasticity affect variation in sexual
size dimorphism in insects: from physiology to evolution. Ann Rev
Entomol 55:227245
Suter RB (1990) Determinants of fecundity in Frontinella pyramitela
(Araneae, Linyphiidae). J Arachnol 18:263269
Van Buskirk J, Steiner UK (2009) The fitness costs of developmental
canalization and plasticity. J Evol Biol 22:852860
Vollrath F (1980) Male body size and fitness in the web-building spider
Nephila clavipes. Z Tierpsychol 53:6178
West-Eberhard MJ (2003) Developmental plasticity and evolution .
Oxford University Press
Yeh PJ, Price TD (2004) Ad aptive p henot ypi c plastici ty an d the
successful colonization of a novel environment. Am Nat 164:
531542
Naturwissenschaften
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... As the spatial scale of urban heating matches the spatial scale at which size reduction is observed (Kaiser et al., 2016;Merckx et al., 2018), the Urban Heat Island effect provides a valid explanation for the observed patterns (Merckx et al., 2018; but see Entling, Schmidt-Entling, Bacher, Brandl, & Nentwig, 2010;Puzin, Leroy, & Pétillon, 2014). However, the impact of small temperature changes on spider body size remains to be studied, and resource availability during development is a well-documented influence and a potentially stronger driver of spider adult size (DiRienzo & Montiglio, 2016;Kralj-Fišer et al., 2014;Mayntz et al., 2003). Higher prey abundance in urbanized spots of the Sydney area was for instance associated with a larger body size in the spider Nephila plumipes (Lowe, Wilder, & Hochuli, 2014. ...
... This suggests that traits that successfully responded at this scale (namely web surface) are more important to prey capture success and biomass gain than the others (mesh width) (Blackledge & Eliason, 2007). Conversely, benefits, costs and trade-offs associated with increased silk production may be detectable in other life-history dimensions than the ones we explored in the present study, such as development time and adult longevity (both expected to increase with resource restriction ;Kleinteich et al., 2015;Kralj-Fišer et al., 2014), or dispersal, which is strongly counter-selected in urban fragmented environments for passively dispersing organisms (Cheptou, Carrue, Rouifed, & Cantarel, 2008). ...
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1.In animals, behavioural responses may play an important role in determining population persistence in the face of environmental changes. Body size is a key trait central to many life history traits and behaviours. Correlations with body size may constrain behavioural variation in response to environmental changes, especially when size itself is influenced by environmental conditions. 2.Urbanization is an important human‐induced rapid environmental change that imposes multiple selection pressures on both body size and (size‐constrained) behaviour. How these combine to shape behavioural responses of urban‐dwelling species is unclear. 3.Using web‐building, an easily quantifiable behaviour linked to body size, and the garden spider Araneus diadematus as a model, we evaluated direct behavioural responses to urbanization and body size constraints across a network of 63 selected populations differing in urbanization intensity. We additionally studied urbanization at two spatial scales to account for some environmental pressures varying across scales and to obtain first qualitative insights about the role of plasticity and genetic selection. 4.Spiders were smaller in highly urbanized sites (local scale only), in line with expectations based on reduced prey biomass availability and the Urban Heat Island effect. Web surface and mesh width decreased with urbanization at the local scale, while web surface also increased with urbanization at the landscape scale. The latter two responses are expected to compensate, at least in part, for reduced prey biomass availability in cities. The use of multivariate mixed modelling reveals that although web traits and body size are correlated within populations, behavioural responses to urbanization do not appear to be constrained by size: there is no evidence of size‐web correlations among populations or among landscapes, and web traits appear independent from each other. 5.Our results demonstrate that responses in size‐dependent behaviours may be decoupled from size changes, thereby allowing fitness maximisation in novel environments. The spatial scale at which traits respond suggests contributions of both genetic adaptation (for web investment) and plasticity (for mesh width). Although fecundity decreased with local‐scale urbanization, Araneus diadematus abundances were similar across urbanization gradients; behavioural responses thus appear overall successful at the population level. This article is protected by copyright. All rights reserved.
... This implies that high variability in life histories may be a consequence of phenotypic plasticity, i.e. the ability of a single genotype to produce alternative phenotypes in response to environmental conditions (West-Eberhard 2003). In arthropods, developmental plasticity can be induced by environmental variables such as diet quality or quantity (Esperk et al. 2007;Kralj-Fišer et al. 2014), temperature (Li and Jackson 1996;Stillwell and Fox 2009), and photoperiod (Schaefer 1977;Leimar 1996). ...
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Adult body size, development time, and growth rates are components of organismal life histories, which crucially influence fitness and are subject to trade-offs. If selection is sex-specific, male and female developments can eventually lead to different optimal sizes. This can be achieved through developmental plasticity and sex-specific developmental trajectories. Spiders present suitable animals to study differences in developmental plasticity and life history trade-offs between the sexes, because of their pronounced sexual dimorphism. Here, we examine variation in life histories in the extremely sexually size dimorphic African hermit spider (Nephilingis cruentata) reared under standardized laboratory conditions. Females average 70 times greater body mass (and greater body size) at maturity than males, which they achieve by developing longer and growing faster. We find a small to moderate amount of variability in life history traits to be caused by family effects, comprising genetic, maternal, and early common environmental effects, suggesting considerable plasticity in life histories. Remarkably, family effects explain a higher variance in male compared to female life histories, implying that female developmental trajectories may be more responsive to environment. We also find sex differences in life history trade-offs and show that males with longer development times grow larger but exhibit shorter adult longevity. Female developmental time also correlates positively with adult body mass, but the trade-offs between female adult mass, reproduction, and longevity are less clear. We discuss the implications of these findings in the light of evolutionary trade-offs between life history traits.
... Although some taxa exhibit significant developmental plasticity (e.g. Esperk et al., 2007), others have a rather canalized development and express low ability for phenotypic changes in response to environmental conditions (Kralj-Fišer et al., 2014). To complicate things further, species often have both plastic and canalized life-history traits. ...
... Although some taxa exhibit significant developmental plasticity (e.g. Esperk et al., 2007), others have a rather canalized development and express low ability for phenotypic changes in response to environmental conditions (Kralj-Fišer et al., 2014). To complicate things further, species often have both plastic and canalized life-history traits. ...
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Variation in life-history traits within a population is caused by genetic, maternal and environmental factors. We explored the high variability in development time, adult body weight and fecundity in females of the sexually size dimorphic spider Trichonephila senegalensis. Their mothers originated from two habitats—strongly seasonal Namibia and mildly seasonal South Africa—and we reared F1 females under standardized laboratory conditions. We found that a considerable part of the variability in recorded life-history traits is caused by family-specific effects, comprising genetic, maternal and early environmental influences. Furthermore, we show population differences in development time, where females originating from Namibia matured within shorter periods than females from South Africa. Also, the relationship between development time and adult weight differs between the two populations, as a significant correlation is only found in females with Namibian origin. Against common wisdom, there was a weak overall correlation between adult weight and clutch mass. We also found that females make different life-history decisions under increasing rather than under decreasing daylength. Although a considerable part of variability in life-history traits is family-specific, we discuss how the between-population differences in life histories and their trade-offs reflect adaptation to diverse habitats.
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Selection forces often generate sex-specific differences in various traits closely related to fitness. While in adult spiders (Araneae), sexes often differ in colouration, body size, antipredator or foraging behaviour, such sex-related differences are less pronounced amongst immatures. However, sex-specific life-history strategies may also be adaptive for immatures. Thus, we hypothesized that, among spiders, immature individuals show different life-history strategies that are expressed as sex-specific differences in body parameters and behavioural features, and also in their relationships. We used immature individuals of a protandrous jumping spider, Carrhotus xanthogramma, and examined sex-related differences. Results showed that males have higher mass and larger prosoma than females. Males were more active and more risk-tolerant than females. Male activity increased with time, and larger males tended to capture the prey faster than small ones, while females showed no such patterns. However, females reacted to the threatening abiotic stimuli more with the increasing number of test sessions. In both males and females, individuals with better body condition tended to be more risk-averse. Spiders showed no sex-specific differences in inter-individual behavioural consistency and in intra-individual behavioural variation in the measured behavioural traits. Finally, we also found evidence for behavioural syndromes (i.e. correlation between different behaviours), where in males only the activity correlated with the risk-taking behaviour, but in females all the measured behavioural traits were involved. The present study demonstrates that C. xanthogramma sexes follow different life-history strategies even before attaining maturity.
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Urbanization in North America has replaced many pre-existing natural environments with artificial, human-populous environments of low biodiversity. Although some bat species have persisted in urban environments, the overall abundance and diversity of bats within them is low. We examined five factors that may contribute to the low diversity of bats in temperate, North American urban environments: anthropogenic noise, road infrastructure and traffic, ecological light pollution, plant roost availability and diversity and the distribution and diversity of prey. We present a review of available literature to evaluate how each factor may constrain bat abundance and diversity in urban environments. We found that anthropogenic noise and plant roost availability and diversity were more likely to influence only some species of bats, whereas road infrastructure and traffic, ecological light pollution and the distribution and diversity of prey were likely to influence most species of bats. Generally, the effects of these factors on bats are common among urban environments, but individual species' responses to these characteristics might differ slightly among urban environments. Additional research about the effects of these factors on urban bat ecology, abundance and diversity, combined with the protection and connection of existing natural habitat, and education about bats, would inform efforts to increase the suitability of urban environments for bats.
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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.
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Rapid urbanization has become an area of crucial concern in conservation owing to the radical changes in habitat structure and loss of species engendered by urban and suburban development. Here, we draw on recent mechanistic ecological studies to argue that, in addition to altered habitat structure, three major processes contribute to the patterns of reduced species diversity and elevated abundance of many species in urban environments. These activities, in turn, lead to changes in animal behavior, morphology and genetics, as well as in selection pressures on animals and plants. Thus, the key to understanding urban patterns is to balance studying processes at the individual level with an integrated examination of environmental forces at the ecosystem scale.
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A prominent interspecific pattern of sexual size dimorphism (SSD) is Rensch’s rule, according to which male body size is more variable or evolutionarily divergent than female body size. Assuming equal growth rates of males and females, SSD would be entirely mediated, and Rensch’s rule proximately caused, by sexual differences in development times, or sexual bimaturism (SBM), with the larger sex developing for a proportionately longer time. Only a subset of the seven arthropod groups investigated in this study exhibits Rensch’s rule. Furthermore, we found only a weak positive relationship between SSD and SBM overall, suggesting that growth rate differences between the sexes are more important than development time differences in proximately mediating SSD in a wide but by no means comprehensive range of arthropod taxa. Except when protandry is of selective advantage (as in many butterflies, Hymenoptera, and spiders), male development time was equal to (in water striders and beetles) or even longer than (in drosophilid and sepsid flies) that of females. Because all taxa show female‐biased SSD, this implies faster growth of females in general, a pattern markedly different from that of primates and birds (analyzed here for comparison). We discuss three potential explanations for this pattern based on life‐history trade‐offs and sexual selection.
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Males and females of nearly all animals differ in their body size, a phenomenon called sexual size dimorphism (SSD). The degree and direction of SSD vary considerably among taxa, including among populations within species. A considerable amount of this variation is due to sex differences in body size plasticity. We examine how variation in these sex differences is generated by exploring sex differences in plasticity in growth rate and development time and the physiological regulation of these differences (e.g., sex differences in regulation by the endocrine system). We explore adaptive hypotheses proposed to explain sex differences in plasticity, including those that predict that plasticity will be lowest for traits under strong selection (adaptive canalization) or greatest for traits under strong directional selection (condition dependence), but few studies have tested these hypotheses. Studies that combine proximate and ultimate mechanisms offer great promise for understanding variation in SSD and sex differences in body size plasticity in insects.
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To investigate the consequences of canalization and plasticity in arthropod developmental pathways, we developed a model that predicts eight possible combinations among three larval developmental parameters. From the descriptions of insect and spider postembryonic development, it is apparent that not all aspects of juvenile development are plastic and that species differ in which traits are plastic. Most strikingly, only four of the possible eight combinations of canalized and plastic parameters have been found in nature. Using this model, we show that the identity of the canalized developmental parameters and the degree of genetic variation in the value at which a given parameter is fixed have important implications for the ecology and evolution of complex life cycles.
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Lycosa T-insignita BOES. et STR. was reared under three different feeding conditions for invetigating the instar numbers and the carapace width growth. The number of instars necessary to maturity was variable with the feeding condition, i.e. it and its variation tended to be increased and much wider respectively as the interval of food supply was prolonged from the every day feeding to the fourth day feeding. Nymphal period was also extended by food supply at longer intervals. The growth curve of carapace width did not fit with that expected from DYAR'S law. The growth of carapace width was almost accomplished by moulting, and further a very small growth was found even within each instar, but not significant statistically. In comparison between adults which passed the same number of moults under different feeding conditions, the final carapace width in the individuals of every fourth day feeding was smaller than in those of every day feeding. From the frequency distribution, it was noticed that the carapace width measurement dit not give an accurate indicator for determining the instar of nymphs, excepting the first and the second instars. The carapace width distribution of field specimens was somehow similar to that of every fourth day feeding in the laboratory, suggesting poor feeding condition in the field. © 1968, JAPANESE SOCIETY OF APPLIED ENTOMOLOGY AND ZOOLOGY. All rights reserved.
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The relationship between body size and web design was studied for the nocturnal orbweaving spider Nuctenea sclopetaria. Body measurements (carapace width, leg length, body length and wet weight) taken from 27 adult female and 22 juvenile spiders were related to web dimensions (capture area, number of radii, capture thread length, mesh height) each spider constructed. Carapace width was found to be the most reliable size measure for predicting web dimensions for adult and juvenile spiders. The study also found that the webs showed a distinct asymmetry due to the enlargement of the lower web half and the extent of this asymmetry increased with carapace width. Furthermore, mesh height increased with distance from the hub. The possible effects of web asymmetry on the prey capture success of spiders are discussed.
Chapter
This chapter states that innovative behaviours are of considerable importance for understanding the ecology and, in turn, the evolution of animals. From an ecological perspective, innovatory propensity may influence biodiversity patterns through its influence on some of the processes that determine the gain and loss of species within the community. From an evolutionary standpoint, it may affect the rate of evolutionary divergence by altering the selective pressures to which individuals are exposed. The growing needs to understand the consequences of innovative behaviours and novel improvements in methods to measure innovation have stimulated a number of recent studies. Here, the chapter uses these new advances to illustrate the importance of behavioural innovation in some of the ecological and evolutionary processes that govern biodiversity. It examines the adaptive value of behaving in a flexible way and discusses new developments in the methods of quantifying innovatory capacity. The chapter further presents a series of comparative studies that seek to understand the role of this capacity in three different biological processes: the invasion of new environments, the risk of extinction, and the rate of evolutionary diversification.