Aging and foraging efficiency in an orb-web spider

Abstract

Aging is often associated with reduced behavioral performance such as decreased locomotion or food consumption, related to a deterioration in physiological functions. In orb-web spiders, webs are used to capture prey and aging can affect web-building behavior and web structure. Here, we investigated the effect of aging on prey capture in the orb-web spider Zygiella x-notata. The ability of adult females to capture flies was examined at different ages. The rate of prey capture did not change with age, but older spiders took more time to subdue and capture the prey. Alterations which appeared in web structure with age (increase in the number of anomalies affecting radii and capture spiral) affected prey capture behavior. Furthermore, the analysis of individual performance (carried out on 17 spiders at two different ages) showed that older females spent more time handling the prey and finding it in the web. Our results suggest that, in the laboratory, age does not affect prey capture rates but it influences prey capture behavior by affecting web structure or/and spider motor functions.

Full text

ARTICLE
Aging and foraging efficiency in an orb-web spider
Myle
`ne Anotaux •Camille Toscani •
Raymond Leborgne •Nicolas Cha
ˆline •
Alain Pasquet
Received: 24 March 2013 / Accepted: 25 April 2014
ÓJapan Ethological Society and Springer Japan 2014
Abstract Aging is often associated with reduced behav-
ioral performance such as decreased locomotion or food
consumption, related to a deterioration in physiological
functions. In orb-web spiders, webs are used to capture prey
and aging can affect web-building behavior and web struc-
ture. Here, we investigated the effect of aging on prey capture
in the orb-web spider Zygiella x-notata. The ability of adult
females to capture flies was examined at different ages. The
rate of prey capture did not change with age, but older spiders
took more time to subdue and capture the prey. Alterations
which appeared in web structure with age (increase in the
number of anomalies affecting radii and capture spiral)
affected prey capture behavior. Furthermore, the analysis of
individual performance (carried out on 17 spiders at two
different ages) showed that older females spent more time
handling the prey and finding it in the web. Our results
suggest that, in the laboratory, age does not affect prey
capture rates but it influences prey capture behavior by
affecting web structure or/and spider motor functions.
Keywords Aging Prey capture efficiency Orb-web
spider Web structure Zygiella x-notata
Introduction
Aging is a progressive natural process in which deteriora-
tion of physiological functions is often associated with
deficits in behavioral performance, which ultimately lead
to death (Arking 1998). Many studies on vertebrate models,
both in the laboratory and natural populations, have led to a
better understanding of aging mechanisms and its conse-
quences for the organism (Austad and Fischer 1991;
Holmes and Austad 1995; Perret and Aujard 2006; Ricklefs
2010). In invertebrates, dipterans such as Drosophila
melanogaster have been used extensively to study age-
related behavioral changes (Grotewiel et al. 2005; Simon
et al. 2006; Lliadi and Boulianne 2010; Jones and
Grotewiel 2011). Most of the aging studies in flies focused
on the decline in behavioral functions linked with age,
including memory, olfaction, and biological rhythms (for
review, see Grotewiel et al. 2005). Furthermore, several
studies have demonstrated a decrease in locomotion with
increasing age in insects (Le Bourg and Minois 1999;
Ridgel et al. 2003). This loss in mobility could influence an
animal’s ability to acquire resources. Food intake is one of
the vital functions that decrease with age. In mammals,
aging is also associated with declines in food consumption
(quantity and quality ingested) (Blanton et al. 1998; McCue
1995). Increasing age has also been shown to be associated
with a decrease in foraging efficiency in the honeybee
Apis mellifera (Tofilsky 2000) and other invertebrates
(Grotewiel et al. 2005; Moya-Larano 2002). However,
none of these studies examined the link between locomotor
abilities and foraging efficiency in aging animals. Orb-web
M. Anotaux and C. Toscani equally contributed to this study.
M. Anotaux (&)R. Leborgne A. Pasquet
Laboratoire Expression et Evolution des Comportements,
Faculte
´des Sciences et Techniques, Universite
´de Lorraine, BP
239 Bld des Aiguillettes, 54506 Vandoeuvre-Les-Nancy, France
e-mail: m.anotaux@voila.fr
C. Toscani (&)
Ecole nationale ve
´te
´rinaire d’Alfort, UMR 7179 CNRS MNHN,
Universite
´Paris-Est, 94704 Maisons-Alfort, France
e-mail: toscani.camille@hotmail.fr
N. Cha
ˆline
Laboratoire d’Ethologie Expe
´rimentale et Compare
´e EA 4443,
Universite
´Paris 13, 99 avenue J.B. Cle
´ment,
93430 Villetaneuse, France
123
J Ethol
DOI 10.1007/s10164-014-0404-6

spiders can be used for this purpose because there is a
direct link between locomotor activity and prey capture
efficiency (Foelix 2011). In fact, spiders first use their legs
(and their whole body) to build a web that will intercept
prey and second to capture prey according to a specific
behavioral sequence of capture (go to the prey, catch it,
immobilize it, and, for some spiders, transport it) (Foelix
2011). Web construction and prey capture are thus two
complementary aspects of orb-spider foraging behavior.
Orb-web spiders are sit-and-wait predators that, unlike
Lycosidae or Salticidae spiders, do not actively search for
prey but instead invest time and energy in the construction
of an orb-web, a geometrical structure which serves as a
trap for prey capture (Heiling and Herberstein 2000; Scharf
et al. 2011). Once the web is built, the spiders wait in the
center or hide in a retreat until a prey strikes the structure.
Prey capture efficiency depends on the orb-web capacity to
(1) intercept prey, (2) inform the spider about the location
of the prey, (3) retain prey long enough for the spider to
subdue it before it escapes or tumbles away, and (4) on the
spider’s capture behavior after prey interception (Coslov-
sky and Zschokke 2009; Sensenig et al. 2011). These
capture abilities depend on silk properties and on the
amount of silk invested for web construction (capture
thread length, capture area) as well as on the arrangement
of the radii and capture threads (Vollrath 1992; Foelix
2011; Harmer et al. 2011). The arrangement of radii and
capture threads is particularly important for successful
capture because, when the spider hides in a retreat at the
edge of the web, silky threads serve to intercept and retain
the prey by absorbing the energy of the struggling prey
without breaking. Vibrations are also transmitted by radii
and a signal thread connecting the center of the web to the
retreat (Zschokke 2000). Recently, we demonstrated that
aging affects orb-web structure. Webs built by old spiders
are smaller, geometrically less regular, and have more
anomalies than webs built by younger spiders (Anotaux
et al. 2012); we suggested that these web modifications
could be due to a decline in spider mobility during web
construction and/or in neurological function.
In this study, we used the orb-web spider Zygiella x-
notata (Araneae, Araneidae, Clerk) to test the effects of age
on foraging efficiency. In this species, spiders build an orb-
web and then wait for a prey in a retreat. When a prey
strikes the web, the spider captures it by following a
characteristic capture behavioral sequence: after
approaching the prey, it immobilizes it by biting and
wrapping it with silk, then it transports the prey to the
retreat to consume it. By comparing prey capture sequen-
ces, their duration and the frequency of their different
components with age, we expect that (1) the rate of prey
capture decreases with aging, (2) the duration of the
behavioral acts increases, and (3) the access to prey and
prey manipulation to subdue it is more difficult.
Materials and methods
Zygiella x-notata is a widespread medium-sized spider
(carapace width for adult females: 1.5 mm) in northern
Europe, which builds its web preferentially in the vicinity
of human buildings. It constructs an orb-web, which is
generally characterized by the presence of a free sector in
the upper part (Fig. 1), and feeds primarily on flying prey
(generally Diptera). In eastern France, its development
cycle is annual: the juveniles leave the eggs sacs at the
beginning of spring, reproduction starts in summer with
mating, females lay eggs in September–October, and
juveniles hatch 3 weeks later and stay in cocoons until
spring. While males die after reproduction, the majority of
Fig. 1 An orb-web built by
Zygiella x-notata. The standard
method used by the spider to
reach the prey (here represented
by the fly Lucilia caesar in the
middle of the lower section of
the web) is shown in red.An
example of an anomaly is also
shown (i.e. discontinuous
thread)
J Ethol
123

females disappear when winter arrives, but some can sur-
vive to the next spring (Jones 1983; The
´venard et al. 2004;
Bel-Venner and Venner 2006). Once adult, the lifespan of
females is approximately from 5 to 7 months (Juberthie
1954; The
´venard et al. 2004).
The spiders used in this study were captured as subad-
ults (in August and September) and reared in the laboratory
in plastic boxes (10 9792.5 cm). They were sprayed
with water and fed once a week with a fly (Lucilia caesar).
They had their last meal 4 days before the tests. All the
spiders used for the tests molted and became adults in the
laboratory, so their exact adult age was known. They were
all virgin females.
Since the body mass of spiders may influence web
construction characteristics and varies with age (Venner
et al. 2003), spiders were weighed before being placed in
experimental conditions (balance: Sartorius BASIC
BA110S, precision 0.1 mg).
Procedure
To collect data on prey capture efficiency, spiders were
placed individually into wooden frames (50 950 9
10 cm) closed by two windowpanes in which they could
build their web. Frames were incubated under controlled
conditions (temperature 20°–22°, hygrometry 55 %, and
luminous cycle of 12 h, light from 0800 to 2000 hours) for
72 h. The spiders were then put back into their respective
boxes once they had made a web or after a maximum of
72 h even if they had not constructed a web. The presence
of a web was checked every day. As soon as a spider
completed a web, the frame was opened and web param-
eters were directly measured using electronic callipers.
Photos (Lumix FZ18 camera) were taken by placing webs
in front of a black panel using artificial light.
After web measurements, we carried out a prey capture
trial. For this, a living prey was placed in the middle of the
lower section of the web (Fig. 1) and then we observed and
quantified spider capture behaviors. The prey used was a
fly (Lucilia caesar) of smaller size than the spider but that
could be considered as a large prey for this spider species
(prey size approximately 2/3 of the spider size and with a
weight of 25 ±5 mg). The observations of spider behavior
began once the prey became entangled in the web.
Parameters
Web parameters
From direct measurements, we estimated the spider’s
investment in the web by calculating the total length of the
capture spiral (capture thread length, CTL) (following
Venner et al. 2000,2001 method).
Anomalies
Anomalies in web construction were identified on photos
and counted (as defined by Pasquet et al. 2013; Fig. 2).
Anomalies can affect the radii or capture spiral, which is the
silky area defined by the presence of sticky threads. For
radii, we counted: the number of supernumerary, deviated,
and ‘‘Y’’ radii (Pasquet et al. 2013; Fig. 2a). For the capture
spiral, we counted the number of stops and returns, holes,
silk threads of the capture spiral stuck together between two
radii, and the number of nonparallel and discontinuous silk
threads in the capture spiral (Pasquet et al. 2013; Fig. 2b).
Prey capture parameters
Before placing the prey in the web, all spiders were in the
same position: they were all in their retreat with a foreleg
(L1) in contact with a signal thread (Fig. 1). We took into
account the following parameters:
–Contact latency Its first movement characterizes the
first reaction of the spider after the prey is introduced
into the web; contact latency is the time between this
first movement and the first contact with the prey. In
general, the spider reaches the prey following the
sequence: retreat, signal thread, center of the web and
prey (see Fig. 1).
–Handling time Handling is a spider behavior (bites and
wrappings) used to subdue the prey. Handling time
begins after the first contact between the spider and the
prey and stops when the spider leaves the capture site
with or without the prey.
–Number of bites A bite is characterized by the
introduction of the spider’s fangs into the prey. A
spider can bite the prey several times during a capture
before it finds a suitable site (i.e. articulation of the prey
or specific places with a thinner cuticle). A bite stops
when the spider’s fangs leave the prey. The number of
bites was noted. There was no way of knowing whether
a spider bite was associated with an injection of venom.
–Number of wrappings Wrapping is a special behavior
during which the spider uses silk to immobilize the
prey. During this behavior, the silk is extruded from the
spinnerets and projected onto the prey; it is visible and
easy for the observer to count the number of wrapping
sequences. This behavior may be reproduced several
times during a capture. For each prey capture, we took
into account the number of wrappings.
–Prey transport time After subduing the prey, the spider
then transports it to its retreat before ingestion. To
transport the prey back to the retreat, the spider hangs it
on its spinnerets. Several events can interrupt the
transport on the way back: the prey can become
J Ethol
123

entangled in the sticky spiral and the spider can lose it,
or the spider can go the wrong way and not find the best
way back to its retreat. The spider might also return to
its retreat without the prey and stay motionless before
coming back and going on with its previous activity.
Each interruption during its return to the retreat was
counted, and the total duration of all interruptions was
included in the time of transport, which ended when the
spider reached its retreat with the prey.
–Activity time This is the total time during which the
spider was actively capturing the prey. This was
calculated by adding the contact latency, the handling
time, and the transport time.
Statistical analyses
Variation in predatory performance with age could be
observed at two different levels: the inter-individual level
between spiders of different ages or the intra-individual
level by comparing the capture performance of spiders at
two different ages.
For the inter-individual analysis, a total of 78 spiders
(aged from 17 to 261 days) weighing between 12 and
73 mg were used. Multiple linear regressions, using the
‘lm’ function of the ‘nlme’ package (Pinheiro et al. 2005)
for R (v.2.15.0), were performed where (1) age and body
mass were the independent variables and web parameter
Fig. 2 a The different type of
radius anomalies defined for
Zygiella x-notata orb-webs
(from Pasquet et al. 2013). A
‘super-numerary radius’ takes
its origin from a spiral thread
unit and not from the center of
the web; a ‘deviated radius’
presents a deviation [5°
compared to a rectilinear
trajectory; a ‘Y’ radius is a
radius separated abnormally
into two radii. bThe different
types of capture spiral
anomalies defined for Zygiella
x-notata orb-webs (Pasquet
et al. 2013). A ‘return’ is when
two spiral units end in one point
(triangular ending) or two points
(rectangular ending) of a radius,
interrupting the spiral; a ‘hole’
is defined by the absence of at
least one spiral unit between
two adjacent spiral units; ‘two
or more spiral units stuck
together’ and ‘discontinuity of
the spiral’ define anomalies of
interruptions in the capture
spiral; ‘non-parallel spiral units’
defines a spiral thread stuck to
another one on a radius, forming
a triangle
J Ethol
123

was the dependant variable, and (2) age, body mass, CTL,
number of anomalies affecting radii, and number of
anomalies of the capture spiral were the independent
variables and each prey capture parameter was the depen-
dant variable. In the tables showing the results of multiple
linear regression analysis, the multiple regression coeffi-
cient ‘‘b’’ referred to a non-standardized coefficient, and
‘‘ b’’ to a standardized coefficient.
In the second analysis, we compared the performance of
17 spiders tested at two different ages. The spiders used in
this analysis were at least 50 days older between test 1 and
test 2 (age of the spiders for test 1: mean =109 ±19 days;
and age for test 2: mean =197 ±33 days). The age of the
laboratory-reared spiders in test 1 was similar to that reached
by adult females in natural conditions (Bel-Venner and
Venner 2006), whereas the age of the spiders in test 2 was
much higher than the average age in natural conditions. To
take into account repeated measurements for each spider,
linear mixed-effects regression models, using the ‘lmer’
function of the ‘lme4’ package (Bates et al. 2013) for R, were
carried out where (1) age and body mass were the indepen-
dent variables, and web parameters were the dependant
variables, and (2) age, body mass, CTL, number of anomalies
affecting radii, and number of anomalies of the capture spiral
were the independent variables, and each prey capture
parameter was the dependant variable. Random individual
effects accounted for repeated measures. The final restricted
maximum-likelihood model, including only significant
effects, was achieved by deletion of the non-significant
interactions and additive effects from the primary model
using the backward stepwise method. Ftests of the signifi-
cance of effects were computed with models derived from
the final model. Pvalues for each effect were obtained by
likelihood ratio tests of the full model with the effect in
question against the model without the effect in question.
A Shapiro–Wilk test was applied to determine whether
the sample data were likely to derive from a normally
distributed population. Most variables were not normally
distributed, thus most prey capture parameters were loga-
rithmically transformed. The normality of model residuals
was verified by calculating a Q–Q plot and a Q–Q line.
Significance was considered at p\0.05.
Results
Variation in the predatory performance with age
at Inter-individual level
Relationship between age and web properties
All 78 webs constructed by the spiders retained the prey
deposited in the lower region of the web. Thus, the rate of
prey capture by web retention was 100 %. The two-pre-
dictor model was able to account for 20 % of the variance
in CTL (F
2,75
=9.51, p\0.001, R
2
=0.20). Body mass
had a significant positive coefficient, indicating that spiders
with higher body mass are expected to build webs with a
longer CTL (Table 1). Spider age had a significant negative
coefficient, indicating that older spiders built smaller webs
(Fig. 3). Multiple linear regression analysis, with capture
spiral anomalies (F
3,69
=1.19, p=0.32, R
2
=0.05) or
radius anomalies (F
3,69
=0.35, p=0.79, R
2
=0.02),
found that none of the independent variables contributed to
the multiple regression models.
Relationship between age and prey capture parameters
Since all spiders successfully caught the prey, the rate of
capture due to capture behavior was 100 %. Multiple linear
regression analysis was conducted to examine the rela-
tionship between prey capture behavior—contact latency,
handling time, number of bites, number of wrappings,
transport time, and activity time—and five potential pre-
dictors—age and spider body mass, CTL, number of cap-
ture spiral anomalies, and number of radius anomalies. The
best model for predicting the contact latency only included
the independent variables: body mass, age, number of radii
Table 1 Results of linear regression analyses of variance of CTL
Variable Multiple regression coefficients t
bb
Intercept 469.164 6.35***
Body mass 5.59 0.31 2.80**
Age -1.68 -0.45 -4.10***
** p\0.01, *** p\0.001
Fig. 3 Partial regression plot for the dependent variable CTL and the
independent variable age
J Ethol
123

anomalies, and the interaction between body mass and age
(F
4,68
=2.07, p=0.09, R
2
=0.11). Only the number of
radius anomalies had a significant positive coefficient,
indicating that the spider needed more time to detect the
prey when there was a higher number of radii anomalies
(Table 2; Fig. 4).
To predict the variance in handling time, only the
number of radius anomalies was removed, and the four
predictor model was able to account for 30 % of the var-
iance in handling time (F
4,65
=7.06, p\0.001,
R
2
=0.30). Body mass and CTL had significant negative
coefficient, indicating that spiders with higher body mass
or who built webs with a higher CTL were expected to
handle prey for shorter periods (Table 3; Fig. 5).
The two predictors used in the best model accounted for
10 % of the variance of the transport time (F
2,74
=3.90,
p=0.02, R
2
=0.10). Body mass had a significant nega-
tive regression coefficient, indicating that larger spiders
spent less time transporting their prey (Table 4).
In contrast, age had a significant positive coefficient,
indicating that older spiders transport their prey more
slowly (Fig. 6). When multiple linear regression analysis
was carried out with bite number and the number of
wrappings, none of the independent variables contributed
to the multiple regression models.
Only three of the independent variables were used in the
best model and these were able to explain 31 % of the
variance of the activity time (F
3,74
=11.06, p\0.001,
R
2
=0.31). Once again, body mass and CTL had signifi-
cant negative regression coefficient, indicating that spiders
with higher body mass or who made webs with a higher
CTL were expected to be active for shorter time periods
(Table 5). Age had a significant positive coefficient,
Table 2 Results of linear regression analyses of variance of contact
latency
Variable Multiple regression
coefficients
t
bb
Intercept -1.74e-01 -1.10
Body mass 7.77e-03 0.53 1.70
Age 1.63e-03 0.56 1.62
Number of radius anomalies 1.46e-02 0.29 2.41*
Body mass:age -4.48e-05 -0.85 -1.64
*p\0.05
Fig. 4 Partial regression plot for the dependant variable contact
latency and the independent variable number of radius anomalies
Table 3 Results of linear regression analyses of variance of handling
time
Variable Multiple regression
coefficients
t
bb
Intercept 2.64 23.14****
Body mass -0.62e-02 -0.31 -2.63**
Age 0.26e-03 0.06 0.53
Number of capture spiral
anomalies
-0.28e-02 -0.18 -1.69*
CTL -0.37e-03 -0.32 -2.74***
*p\0.05, ** p\0.01, *** p\0.001, **** p\0.0001
Fig. 5 Partial regression plot for the dependant variable handling
time and the independent variable CTL
Table 4 Results of linear regression analyses of variance of transport
time
Variable Multiple regression coefficients t
bb
Intercept 1.171 5.50***
Body mass -0.014 -0.67 -2.48*
Age 0.002 0.46 2.07*
*p\0.05, *** p\0.001
J Ethol
123

suggesting that older spiders were active for longer periods
of time (Fig. 7).
Variation in the predatory performance with age
at the intra-individual level
Relationship between age and web properties
Linear mixed-effect analysis was used to study the effects
of age and body mass on web parameters (CTL, number of
capture spiral anomalies and number of radius anomalies)
for spiders at two different ages. None of the predictors,
however, was able to explain the variance in the dependent
variables.
Relationship between age and prey capture properties
Linear mixed-effects regression models showed that there
was a significant association between age and handling
time (v
2
=7.24, p=0.007), with an increase in handling
time of 1.43 ±1.95 s for each day increase in age.
Transport time varied significantly with the number of
radius anomalies (v
2
=16.40, p=0.006), increasing with
the increase in radius anomalies (log, 0.05 ±0.04 s for
each radius anomalies). Age tended to affect transport time
(v
2
=3.52, p=0.06), increasing it by log: 0.07 ±0.01 s
each day. Activity time varied significantly with age
(v
2
=11.80, p\0.001) and CTL (v
2
=4.03, p=0.04),
increasing for each day increase in age (log,
0.020 ±0.005 s) and for each increase in CTL of one cm
(log, 0.007 ±0.001 s). However, none of the predictors
were able to explain the variance in contact latency.
Discussion
In the present study, we examined the effect of age on the
efficiency and behavioral changes in spider foraging.
Contrary to our predictions, the rate of prey capture by
spiders did not differ with age. The prey (flies) was directly
deposited in the web and thus it was perhaps easier for the
spiders to capture it than in nature. Our results showed that
with age there are some changes in time management
during spider capture behavior, and that age-induced
changes in web properties also appeared to have an indirect
effect on these behaviors.
The consequences of aging on behavioral performance
are variable depending on the activity (foraging, repro-
duction, locomotion; Grotewiel et al. 2005). These are
Fig. 6 Partial regression plot for the dependant variable transport
time and the independent variable age
Table 5 Results of linear regression analyses of variance of activity
time
Variable Multiple regression coefficients t
bb
Intercept 2.51 23.77***
Body mass -0.83e-02 -0.37 -3.42**
Age 0.12e-02 0.26 2.33*
CTL -0.04e-02 -0.29 -2.68**
*p\0.05, ** p\0.01, *** p\0.001
Fig. 7 Partial regression plot for the dependant variable activity time and the independent variables age and CTL
J Ethol
123

often linked to a decrease in locomotor activity in ver-
tebrates (i.e. in rats; Altun et al. 2007) and invertebrates
(i.e. in nematodes; Murakami and Murakami 2005), or in
Drosophila (Le Bourg and Minois 1999). In particular,
in Drosophila melanogaster, locomotor behavior, such as
negative geotaxis, exploratory activity, fast phototaxis,
and flight ability, decline with age (Grotewiel et al.
2005). In spiders, it has also been shown that age can
influence locomotor behavior, i.e., Lycosa tarantula,
(Araneae, Lycosidae), an iteroparous species that repro-
duces in two successive years, is more productive in the
first year than in the second (Moya-Larano 2002). Fur-
thermore, in this latter study, the author showed that, in
the second year, females were less active with a lower
locomotor activity than the first-year females. For the
orb-web spider Zygiella x-notata, it was recently shown
that aging affects web geometry, and thus web-building
behavior (Anotaux et al. 2012; Toscani et al. 2012). In
these papers, the authors also suggested that these age-
induced changes in the webs could have a locomotor
origin with an associated degradation of the mechanical
properties of the spiders’ legs.
In our study, activity time during prey capture increased
with age; comparison of prey capture parameters for the
same spider at least 50 days later showed that this increase
in the activity time was due to an increase in handling time.
It is possible that the locomotor behavior used to immo-
bilize the prey becomes more difficult with age because old
spiders tire more rapidly during the struggle with prey than
younger spiders.
It is known that body mass can lead to variations in web-
building behavior (Venner et al. 2003; Kunter et al. 2010)
and foraging effort (Venner et al. 2003). When spider body
mass increased, the amount of silk used per web decreased,
while their foraging effort increased (Venner et al. 2003).
As the feeding conditions were uniform for all spiders used
in our laboratory experiment, body mass should not have
had an effect and cannot explain differences in capture
performance. However, in nature, spiders rarely feed to
satiation and body mass may play an important role in
determining differences in performance in young and old
adults.
We also showed that changes in web construction affect
foraging effort: the activity time increased and spiders took
longer to handle the prey when less silk was used to make a
web. Anotaux et al. (2012) suggested that spiders invest
less silk in their web with aging because aging affects the
glands that produce spiral silk and leads to a reduction in
silk reserves. In our study, it appeared that, to compensate
for the decrease in silk investment, which occurs with age
and can lower the probability of capturing prey by reducing
the capture area, spiders took longer to reach the prey to
ensure that it did not escape.
Our results showed that the contact latency between the
spider and the prey increased with the number of anomalies
affecting radii; spiders took more time to detect the prey
because radii with anomalies do not correctly transmit prey
vibrations, or because spiders are less skilled at moving on
radii affected by anomalies. This could also explain why, in
the intra-individual approach, transport time was found to
increase with the number of anomalies.
We found a significant relationship between mass/age
and some web properties at the inter-individual level but
not in the second approach based on intra-individual rela-
tionships. This difference is probably due to a methodo-
logical problem. For the inter-individual comparison, 78
spiders aged from 17 to 261 days were used whereas, in the
intra-individual comparison, we used only 17 spiders and
the range of ages was reduced (range, 109–197 days) (see
‘‘ Materials and methods’’). Thus in the second case, we
reduced the variability in spider age and mass and this
could explain the absence of a relationship between these
parameters and web properties found in the inter-individual
comparison.
Initially, we expected that prey capture efficiency would
decrease with age. However, the observed changes in
handling behavior and age-induced changes in web
geometry did not alter prey capture rates. Nevertheless, the
time to complete capture behavior activities did increase
with age and access to prey appeared to be more difficult.
These findings therefore suggest that, although in the lab-
oratory aging did not have a dramatic impact on spider
capture performance, in the wild, these age-induced chan-
ges in behavior could affect spider survival due to longer
exposure to predators.
Acknowledgments The University of Nancy supported this work
with a grant to M. Anotaux. The study is supported by a grant of the
CNRS program ‘‘Longe
´vite
´et Vieillissement’’. We thank the
reviewers for their invaluable comments. We also thank J. Marchal
and L. Bahans who helped collect the spiders in 2008 and 2009 and
assisted with spider breeding in the laboratory in 2009. Finally, we
thank Dr. Leigh Gebbie, LGK Australia, for corrections.
References
Altun M, Bergman E, Edstrom E, Johnson H, Ulfhake B (2007)
Behavioral impairments of the aging rat. Physiol Behav
92:911–923
Anotaux M, Marchal J, Cha
ˆline N, Desquilbet L, Leborgne R, Gilbert
C, Pasquet A (2012) Ageing alters spider orb-web construction.
Anim Behav 84:1113–1121
Arking R (1998) The biology of aging: observations and principles.
Sinauer, Sunderland
Austad SN, Fischer KE (1991) Mammalian aging, metabolism, and
ecology: evidence from the bats and marsupials. J Gerontol
46:B47–B53
Bates DM, Maechler M, Bolker B (2013) lme4: linear mixed-effects
models using S4 classes. R package version 0.999999-2
J Ethol
123

Bel-Venner MC, Venner S (2006) Mate-guarding strategies and male
competitive ability: results from a field study in an orb-weaving
spider. Anim Behav 71:1315–1322
Blanton CA, Horwitz BA, Murtagh-Mark C, Gietzen DW, Griffey
SM, McDonald RB (1998) Meal patterns associated with the
age-related decline in food intake in the Fischer 344 rat. Am
Physiol Soc 44(5):R1494–R1502
Coslovsky M, Zschokke S (2009) Asymmetry in orb-webs: an
adaptation to web building costs? J Insect Behav 22:29–38
Foelix RF (2011) Biology of spiders, 3rd edn. Oxford University
Press, Oxford
Grotewiel MS, Martin I, Bhandari P, Cook-Wiens E (2005)
Functional senescence in Drosophila melanogaster. Ageing
Res Rev 4:372–397
Harmer AMT, Blackledge TA, Madin JS, Herberstein ME (2011)
High-performance spider webs: integrating biomechanics, ecol-
ogy and behaviour. J R Soc Interface 8:457–471
Heiling AM, Herberstein ME (2000) Interpretations of orb-web
variability: a review of past and current ideas. Ekol Bratisl
19:97–106
Holmes DJ, Austad SN (1995) The evolution of avian senescence
patterns: implications for understanding primary aging pro-
cesses. Am Zool 35:307–317
Jones D (1983) Guide des Araigne
´es et des Opilions d’Europe.
Delachaux et Niestle
´, Paris
Jones M, Grotewiel MS (2011) Drosophila as a model for age-related
impairment in locomotor and others behaviors. Exp Gerontol
46(5):320–325
Juberthie C (1954) Sur les cycles biologiques des Araigne
´es. Bull Soc
Hist Nat Toulouse 89:299–318
Kunter M, Gregoric M, Li D (2010) Mass predicts web asymmetry in
Nephila spiders. Naturwissenschaften 97:1097–1105
Le Bourg E, Minois N (1999) A mild stress, hypergravity exposure,
postpones behavioral aging in Drosophila melanogaster. Ger-
ontology 34(2):157–172
Lliadi KG, Boulianne GL (2010) Age-related behavioral changes in
Drosophila. Ann N Y Acad Sci 1197:9–18
McCue JD (1995) The naturalness of dying. JAMA 273:1039–1043
Moya-Larano J (2002) Senescence and food limitation in a slowly
ageing spider. Funct Ecol 16:734–741
Murakami S, Murakami H (2005) The effects of aging and oxidative
stress on learning behavior in C. elegans. Neurobiol Aging
26:899–905
Pasquet A, Marchal J, Anotaux M, Leborgne R (2013) Imperfections
in a perfect architecture: the orb web of spiders. Eur J Entomol
110(3):413–500
Perret M, Aujard F (2006) Vieillissement et rythmes biologiques chez
les primates. Me
´d Sci 22:279–283
Pinheiro JC, Bates DM, Debroy S, Sarkar D (2005) Nlme: linear and
non linear mixed-effects models. R package version 3.1-83, R
foundation for statistical computing, Vienna
Ricklefs RE (2010) Insights from comparative analyses of aging in
birds and mammals. Aging Cell 9(2):273–284
Ridgel AL, Ritzmann RE, Scheafer PL (2003) Effects of aging on
behaviour and leg kinematics during locomotion in two species
of cockroach. J Exp Biol 206:4453–4465
Scharf I, Lubin Y, Ovadia O (2011) Foraging decisions and
behavioural flexibility in trap-building predators: a review. Biol
Rev Camb Philos Soc 86(3):626–639
Sensenig AT, Agnarsson I, Blackledge TA (2011) Adult spiders use
tougher silk: ontogenetic changes in web architecture and silk
biomechanics in the orb-weaver spider. J Zool 285:28–38
Simon AF, Liang DT, Krantz DE (2006) Differential decline in
behavioral performance of Drosophila melanogaster with age.
Mech Ageing Dev 127:647–651
The
´venard L, Leborgne R, Pasquet A (2004) Web-building manage-
ment in an orb-weaving spider, Zygiella x-notata: influence of
prey and conspecifics. C R Biol 327:84–92
Tofilsky A (2000) Senescence and learning in honeybee (Apis
mellifera) workers. Acta Neurobiol Exp 60:35–39
Toscani C, Leborgne R, Pasquet A (2012) Analysis of web building
anomalies in the orb weaving spider Zygiella x-notata (Araneae,
Araneidae). Arachnol Mitt 43:79–83
Venner S, Pasquet A, Leborgne R (2000) Web-building behaviour in
the orb weaving spider Zygiella x-notata: influence of experi-
ence. Anim Behav 59:603–611
Venner S, Thevenard L, Pasquet A, Leborgne R (2001) Estimation of the
web’s capturethread length in orb-weavingspiders: determiningthe
most efficient formula. Ann Entomol Soc Am 94(3):490–496
Venner S, Bel-Venner MC, Pasquet A, Leborgne R (2003) Body-
mass-dependant cost of web-building behavior in an orb weaving
spider, Zygiella x-notata. Naturwissenschaften 90:269–272
Vollrath F (1992) Analysis and interpretation of orb spider explora-
tion and web-building behavior. Adv Stud Behav 21:147–199
Zschokke S (2000) Form and function of the orb-web. Eur Arachnol
2002:99–106
J Ethol
123