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Received: 22 October 2021 Revised: 20 December 2021 Accepted: 6 January 2022
DOI: 10.1111/eth.l3268
RESEARCH ARTICLE W I L E Y
Use of conditional prey attack strategies in two generalist
ground spider species
Narmin Beydizada Milan Řezáč2
I Stano Pekár1
department of Botany & Zoology, Faculty
of Science, Masaryk University, Brno,
Czech Republic
2
Biodiversity Lab, Crop Research Institute,
Prague-Ruzyně, Czech Republic
Correspondence
Stáno Pekar, Department of Botany &
Zoology, Faculty of Science, Masaryk
University, Kotlářská 2, 611 37 Brno,
Czech Republic.
Email: pekar@sci.muni.cz
Funding information
International Visegrád Fund; Ministry of
Education, Youth and Sports of the Czech
Republic
Abstract
Generalist predators have evolved a variety of behavioural adaptations in prey capture
to effectively subdue different prey types. Such predators use a conditional hunting
strategy. Among spiders, representatives of Gnaphosidae are known to use either
venom attack (subduing prey with venom) or silk attack (subduing prey with silk). In
this study, we aimed to test the hypothesis of the conditional use of prey capture
strategy (venom versus silk attack) in two species, Drassodes sp. and Zelotes sp. We
also measured the size of their venom glands and the number of their piriform glands
in order to reveal whether behavioural adaptations are paralleled with morphological
ones. As prey, we used other spiders of variable sizes as these are considered dangerous
prey. We found that Drassodes used mainly silk attack, while the majority of
Zelotes used venom attack. The probability of using silk attack increased with predator/prey
body length ratio in Drassodes, but not in Zelotes. Then, we disabled silk use
in individuals of both species. All disabled Drassodes used venom attack, but about
half of individuals attempted to use silk attack first. All Zelotes used venom attack, and
none attempted to use silk attack first. We found significantly larger venom glands
in Drassodes than in Zelotes, while the number of piriform silk glands was similar. The
behavioural adaptations are, thus, not paralleled with morphological (i.e., venom and
silk gland size) ones. Our results suggest that both Drassodes and Zelotes can use both
attack strategies with similar efficacy.
KEYWORDS
Araneae, Drassodes, silk immobilization, venom gland, Zelotes
1 | INTRODUCTION
The behavioural repertoire used in prey searching and prey capture
is often very complex both in generalist vertebrate (e.g., fish, van
Wassenberg et al., 2006; frogs, Valdez & Nishikawa, 1997; lizards,
Lappin & German, 2005) and invertebrate predators (beetle, Murdoch
& Marks, 1973; spiders, Jackson, 1992; Tsai & Pekar, 2019). The fact
that generalist predators can often shift between active (kinematic)
and ambush (si- and-wait) foraging strategies Zoroa et al., 2011; Ross &
Winterhalder, 2015) suggest that such behaviour is also plastic. These
predators have evolved such a repertoire because they deal with a
variety of prey types. To catch a prey, they are expected to select the
most successful capture strategy for a particular prey type from available
alternative strategies (Monroy & Nishikawa, 2011). For example,
the active strategy that maximizes success in capturing small, highly
mobile prey might be much less successful for capturing larger, slowly
moving prey, or prey that is capable of defending itself from predation
(e.g., Lappin & German, 2005; Sherbrooke & Schwenk, 2008). Thus, the
decision of which type of strategy to use is conditioned/optimized also
by many other factors, such as prey defensive characteristic, prey size,
prey density, and the predator's physiological state (van Wassenberg
et al., 2006; Willemart & Lacava, 2017).
Ethology. 2022;00:1-7. wileyonlinelibrary.com/journal/eth © 2022 Wiley-VCH GmbH | 1
Spiders are considered the most diverse group of terrestrial
predators, with foraging behaviour that is largely opportunistic
(Pekar et al., 2012, 2017). Most spider predators are euryphagous
and generalists, and their diets consist mainly of insects and other
arthropods, including other spiders and/or conspecifics (e.g., Heuts
& Brunt, 2001; Guseinov, 2006). Spiders are expected to use a variety
of foraging strategies (Pekar & Toft, 2015), which should result
from complex interactions between the prey and predator (Brodie &
Brodie, 1999). Similarly, as in other generalists, the use of these preycapture
strategies is often conditional upon the type of prey and
its defensive characteristics, particularly dangerousness and size
(Mukherjee & Heithaus, 2013; Tsai & Pekar, 2019). When faced with
several different preys, the spider predator may use different optimal
capture behaviours for each depending not only on the type of
prey but also on the prey-specific balance of costs (Bolnick & FerryGraham,
2002; van Wassenberg et al., 2006). Therefore, generalist
spiders are an excellent model for studying possible conditional foraging
behaviour in prey-predator systems.
Foraging strategy comprises a series of behaviours effective
at different stages of the prey capture sequence, beginning with
approach and ending with attack or immobilization. Conditional
foraging strategies have been reported in a range of spider representatives.
For instance, Yllenus arenarius Menge (Bartos & Szczepko,
2012) used prey-specific capture strategies towards prey, exhibiting
both high and low escape risk. Another intriguing example is
the spitting spider, Scytodes pallida Doleschall, which regulated the
amount of spit depending on the size of prey and its struggling intensity
(Clements & Li, 2005). Portia spiders have capacities (Wilcox &
Jackson, 1998) to use alternative capture strategies, with or without
the use of a web (Jackson & Hallas, 1986). Such switching foraging
behaviour remains little known in other generalist spider predators.
Similarly, spiders of the family Gnaphosidae use two different
capture strategies to immobilize prey: silk or venom attack (Wolff
et al., 2017). Silk attack is a non-contact form of prey immobilization,
while venom attack (and venom injection) requires direct contact between
the predator and prey. In general, silk attack has been broadly
accepted to be more efficient (Pekar & Toft, 2015) and presumably
a safer strategy than venom attack (Gilbert & Rayor, 1985; Schmidt,
1990), especially when the prey is dangerous. However, gnaphosid
spiders are known to often hunt dangerous prey, such as ants or spiders
(Jarman & Jackson, 1986; Michálek et al., 2018), beside other
types of prey (Michálek et al., 2017,2018; Petrákova Dušátková et al.,
2020), which increases the frequency of silk attacks by these spiders.
Frequent silk use in such generalist species has led to the modification
of the spinning apparatus, that is, anterior lateral spinnerets
(ALS) produce sticky silk from the piriform gland (PI) during prey
capture. Our recent comparative analysis of a number of gnaphosid
genera showed that most genera used silk attack to immobilize particularly
large prey, while a few genera used venom attack (Beydizada
et al., 2020). Ancestral state reconstruction revealed that the use of
silk for prey immobilization was as probable as venom attack for ancestors
(Beydizada et al., 2020). It seems that the production of both
silk and venom is costly, so there should be a trade-off in using them,
albeit in differing proportions. Thus, most species using venom attack,
for example, should have larger venom glands than species that
use mainly silk attack. The size of venom glands correlates with body
size and bigger venom glands are characteristic of generalist spiders
(Pekaretal.,2018).
Our aim here was to investigate how fixed the use of a capture
strategy is in generalist ground spider predators of the family
Gnaphosidae. We selected two genera, Drassodes and Zelotes, known
to use different attack strategies with different frequencies (Beydizada
et al., 2020). We performed a manipulative experiment in which the
use of one strategy was disabled. In addition, we also performed measurements
of the venom (size) and silk (number of piriform) glands in
order to reveal whether behavioural adaptations are paralleled with
morphological ones. We predicted that the venom glands would be
larger in species that use them for immobilization and vice versa.
2 | MATERIAL AND METHODS
2.1 | Study species
Specimens of Drassodes sp. (N = 50: 48 juveniles and two subadult
females) and Zelotes sp. (N = 20: 6 juveniles, three subadult females,
three subadult males, and eight adult females) were collected by
hand either under stones or under the bark in the territory of Czechia
(Hady, Brno, August-October, 2020). Zelotes sp. represented a mixture
of Zelotes, Drassyllus, and Trachyzelotes individuals according to
the World Spider Catalog (2021). Collected specimens were placed
singly in Eppendorf tubes (2.5 ml) with punctured lids, placed with
a piece of wet paper tissue in a plastic bag, and transported to the
laboratory. To standardize their satiation level, spiders were fed with
other spiders (see below). If a spider did not capture prey, it was
considered unmotivated to eat (i.e., satiated or preparing to moult),
and those individuals were again offered prey the next day. After
feeding, spiders were kept in a chamber at low temperature (10°C)
and under a short-day regime (LD = 8:16) prior to their use in experiments
in order to slow their ontogenetic development.
As prey, we used spiders (juvenile and subadult stages) of
Pardosa sp. (N = 50), Mangora acalypha (N = 18), and Xysticus sp.
(N = 2). They were collected by hand around the university campus
(Czechia: Brno). Prey spiders were kept singly in plastic containers/
tubes (1.5 ml) with a piece of moist paper tissue. All prey animals
were held under the following conditions: 4°C, LD = 8:16.
All spiders used were identified using the key by Nentwig et al.
(2021). After identification, the prosoma length of all individuals
was measured to the nearest 0.1 mm using an ocular ruler within an
Olympus stereomicroscope.
2.2 | Experimental procedure
One week before using Drassodes (mean prosoma
length ± SEM = 2.67 ± 0.004 mm) and Zelotes (mean prosoma
BEYDIZADAET AL
length ± SEM = 2.22 ± 0.05 mm) in experiments, all spiders were
moved to room temperature (23 ± 1°C). During this period, these
spiders were not fed. Then, Drassodes or Zelotes individuals were
placed singly in Petri dishes (diameter 3.5 cm or 5.5 cm; height
1.5 cm, depending on their body), and the experimental trial began
after at least 1 h of acclimatization. Each individual was offered
one specimen of the prey so that the body size of the prey was
smaller than the body size of the predator. Pardosa spiders (mean
prosoma length ± SEM = 2.19 ± 0.002 mm) were used as prey for
Drassodes. As Pardosa spiders were too large compared to Zelotes,
we used Mangora (mean prosoma length ± SEM = 1.26 ± 0.01 mm)
and Xysticus spiders (mean prosoma length ± SEM = 0.95 ± 0.10 mm)
instead because these were smaller than Zelotes and easily available.
Predator-prey interactions were recorded for up to approximately
60 mins using a video camera (Canon Legria HF R606). Each video
recording began when the prey was released into the dish. The trial
ended when the predator spider had killed and consumed the prey
or when one hour had elapsed.
Then, after six days, the Drassodes individuals were split randomly
into two equal groups, 'sealed' and 'control', each containing
25 individuals. Each individual was anesthetized by means of C 0 2 for
a period of 1-2 minutes and then placed into a dish under a stereomicroscope.
Melted beeswax was applied to the tips of all spinnerets
(the sealed group) or to the ventral side of the abdomen close to the
spinnerets (the control group) by means of fine soldering iron. The
spiders from the sealed group, thus, could not produce silk.
In Zelotes spiders, as the number of individuals was smaller, all
individuals were manipulated. After six days, all Zelotes individuals
were anesthetized (as above), and the tips of their spinnerets were
damaged by pressing them with a fine hard pincer. We could not use
beeswax in Zelotes as their spinnerets were too small.
One day after treatment, the spiders were used in prey-capture
trials. Drassodes and Zelotes spiders were each offered prey that
were approximately 50% smaller in size (i.e., the prey's body length
was similar to the predator's prosoma length, Figure SI). All trials
were conducted in similar environmental (room) conditions as mentioned
above. Drassodes or Zelotes spiders were released singly into
Petri dishes (as above) and left approximately for 1 h to acclimatize.
Then, the prey was released, and the interactions were recorded
using a video camera. Each trial ended when the predator captured
the prey or when one hour had elapsed.
The movies with hunting sequences were analysed (Video SI).
We recorded the capture behaviour used, the hunting success, and
the latency to attack (the period between the first contact with the
prey and the prey attack, either by silk or venom).
2.3 | Venom and silk glands
We measured the size of venom glands and counted the number of
silk glands in juvenile Drassodes (N = 7) and Zelotes (N = 7) individuals.
Spiders were kept in Eppendorf tubes and starved for about
3 days prior to dissection of the glands. To dissect venom glands, the
EKi^^^H f -wi LLY
spiders were first anaesthetized with C 0 2 and then mounted upsidedown
on a paraffin stub by means of a thin pin (pushed through the
posterior part of the prosoma). Then, using fine pincers, the base
of the chelicerae was removed, which released the glands from the
prosoma. Using fine pincers, the dissected glands were placed into a
drop of physiological solution (NaCI 0.9%) on a glass slide. Similarly,
the anterior lateral spinnerets along with their associated silk glands
were dissected from four individuals of both Drassodes and Zelotes.
The number of piriform glands was counted. The dimensions of
the venom glands—the widths (2r) and lengths (d)—were measured
using an ocular ruler in an Olympus SX stereomicroscope. The volume
of the gland (V) was estimated by assuming a cylindrical shape
(V = dnr2
). The length of the prosoma was also measured for each
individual.
2.4 | Statistical analyses
Paired t test with Welch approximation was used to compare latencies
to attack because the variance between the two experimental
groups differed. Mc Nemar's test was used to compare the proportions
of the use of venom attack between experimental groups.
Generalized linear models with binomial error structure (GLM-b)
were used to test the relationship between the prey-to-predator
body size ratio (the ratio of the prosoma length of the prey to the
prosoma length of the spider) and the attack probability separately
for Drassodes and Zelotes (Pekar & Brabec, 2016). The relative volume
of the venom glands and the relative number of silk glands
(i.e., normalized to prosoma length) were compared between species
using GLMM implemented within generalized additive models
from the mgcv package (Wood, 2006). For the venom gland volume,
a gamma error structure was used, while for the number of piriform
glands, Poisson's error structure was used. GLMM was used because
there were two measurements per individual. All statistical analyses
were performed within the R environment (R Core Team, 2017).
3 | RESULTS
3.1 | Venom and silk glands
The relative volume of venom glands was significantly larger in
Drassodes than in Zelotes (GLMM-g, Ft 1 2 = 14.0, p = .001, Figure 1).
The number of piriform glands was not significantly different between
Drassodes and Zelotes after correcting for their prosoma length
(GLMM-p, X2
! < 0.1, p = .84).
3.2 | Prey capture behaviour
Unmanipulated Drassodes and Zelotes spiders used one of three attack
strategies: silk attack followed by biting, that is, the quick immobilization
of prey by silk from a short distance and then biting
prey (observed in both species); venom attack, that is, the prey was
grasped with the forelegs, pulled towards chelicera, and immobilized
using a bite and venom injection (in both species); and venom attack
followed by silk application, that is, the prey was grasped and bitten
and then silk was applied on the legs of prey while the prey was held
in the predator's chelicerae (in Drassodes only). These two strategies
were combined into one, henceforth referred to as 'venom attack'.
All unmanipulated Drassodes individuals captured and consumed
Pardosa prey (N = 50). A great majority of individuals used silk attack
a 0.3
o
>
Drassodes Zelotes
F I G U R E 1 Comparison of venom gland volume between
Drassodes and Zelotes. Blue lines represent the mean, grey boxes
represent 95% confidence intervals of the mean
(Figure 2a). There was a positive relationship between the ratio of
predator/prey length and the use of silk attack (GLM-b, X2
1 = 7.4,
p = .007, Figure 3), that is, as prey size increased compared to
Drassodes size, silk attack was more frequently used.
Similarly, all Drassodes individuals with sealed spinnerets captured
prey (N = 25), and all used venom attack (Figure 2a). However,
40% of individuals tried to use silk attack first. All these individuals
also used silk attack before manipulation. There was no significant
difference in the latency to attack between the unmanipulated and
sealed groups (Paired t-test, t 2 4 = -1.5, p = .146); the attack occurred
on average after 304.1 s (SE = 25.0).
Also, 92% (N = 25) of Drassodes individuals from the control
group captured prey. However, a great majority (N = 21) of individuals
used venom attack (Figure 2a). There was a significant difference
in the frequency of venom attack between the unmanipulated and
control groups (McNemar's test, X2
1 = 8.1, p = .0044), revealing the
effect of experimental manipulation. There was a marginally significant
difference in the latency to attack between unmanipulated and
control groups (Paired t-test, t 2 2 = 2.0, p = .055): the attack occurred
on average after 203.0 s (SE = 20.1). Compared to their capture
behaviour before manipulation, 43% of individuals (N = 23) shifted
from the silk to venom attack, while the remaining individuals used
the same attack behaviour. Only two individuals used venom attack
in both trials.
All unmanipulated Zelotes spiders captured prey (N = 20). The
majority of individuals used venom attack (Figure 2b). There was no
significant relationship between predator/prey size ratio and the use
of venom attack (GLM-b, X2
1 < 0.1, p = .79).
Similarly, all Zelotes individuals with damaged spinnerets captured
prey (N = 20), and all individuals used venom attack (Figure 2b).
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F I G U R E 2 Comparison of relative frequencies of the use of two attack strategies (silk or venom attack) in (a) three experimental groups
of Drassodes and (b) two experimental groups of Zelotes individuals
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F I G U R E 3 Relationship between the probability of using venom
attack for the immobilization of prey and the prey-to-predator
prosoma length ratio in Drassodes. The estimated logit model
is shown with a 95% confidence band (grey area). Rugs along
horizontal axes show binary measurements (0,1)
No individual tried to use silk attack. However, 30% of individuals
shifted from silk (before manipulation) to venom attack, so there
was a significant difference between the groups in the use of venom
attack (McNemar's test, X2
1 = 4.1, p = .04). There was no significant
difference in the latency to attack between unmanipulated and
manipulated groups (Paired t-test, t 3 7 = -1.3, p = .16): the attack occurred
on average after 1055 s (SE = 46.9).
4 | DISCUSSION
We found that the capture strategies are not fixed but exchangeable
in both Drassodes and Zelotes. If the strategies provide similar benefits
and exert similar costs, then we expect them to be used with
similar frequency. The results also show that the results of treatment
(the inability to use silk attack) did not affect the success of
prey-capture, though we did not measure the costs of each strategy.
However, some spiders did not use the available strategy directly
but tried to immobilize the prey by silk. This indicates that silk attack
is a preferred strategy to venom attack probably because it is less
costly.
The use of silk attack increased considerably with the relative
size of the prey in Drassodes, but not in Zelotes. A similar relationship
was observed in other spiders. For instance, in the orb-web
spider of the genus Argiope, prey size determined the structure,
properties, and amount of the silk material used (Murakami, 1983).
We assume that the attack strategy is more plastic and exchangeable
in Drassodes than in Zelotes. For Zelotes, the size of prey may
not be as important as the type of prey which we, however, did not
study here.
It is also interesting to note that the attack strategy of Drassodes
was similar to other gnaphosid generalist spiders, such as Pterotricha,
Scotophaeus, and Gnaphosa, while the attack strategy of Zelotes was
very similar to the attack behaviour observed in Haplodrassus and
Trychothyse (see Beydizada et al., 2020). Pterotricha, Scotophaeus,
and Gnaphosa switched to the silk attack with increasing prey size
as done by Drassodes, whereas Haplodrassus and Trychothyse did
not, which is similar to the behaviour of Zelotes. This indicates a
certain degree of phylogenetic relatedness. However, this prey capture
similarity among genera is not supported by the most recent
phylogenetic analysis of Gnaphosidae. This analysis may not reflect
true phylogenetic relationship as it was based only on morphological
characters (Azevedo et al., 2018), or if it does, then the capture strategy
is highly labile within Gnaphosidae.
There was a remarkable behavioural difference in how Drassodes
and Zelotes responded to the new condition following treatment.
Manipulated Drassodes tried to use silk to immobilize the prey, but
not manipulated Zelotes individuals. We believe that there is some
degree of preference in using either silk or venom among generalist
gnaphosid spiders, although highly modified spinning apparatus
characterizes the whole family Gnaphosidae. We cannot also exclude
the possibility that the difference in the described behaviour
could be because of the different treatment of the spinnerets and
perhaps because of different preys used that possess different locomotory
behaviour. Pardosa is an active hunting spider, while Mangora
is a web-builder, and Xysticus is a sit-and-wait predator.
Recent behavioural as well as morphological investigations of
gnaphosids have shown the anterior lateral spinnerets (ALS) to play
an important role in prey capture, enabling ground spiders to subdue
dangerous prey (Wolff et al., 2017). Indeed, the use of silk is associated
not only with the size of the ALS (which produce sticky silk
from piriform glands) but also with the number of spigots located on
the ALS (Beydizada et al., 2020). Perhaps blocking the function of
only the ALS would be ideal for investigating more exactly the role
of these glands. However, due to the very small size of the studied
specimens, it was too difficult to apply melted beeswax only on certain
spinnerets while leaving other spinnerets untouched. Therefore,
we had to block or damage all spinnerets.
Since the use of both biomaterials, venom and silk, is metabolically
costly, there might be a trade-off in using them. In Drassodes,
the prey is more often immobilized with silk. Thus, we expected that
if less venom is used for prey immobilization, then it is because their
venom glands are smaller. We failed to find support for this prediction.
However, it might not be the venom gland volume but venom
composition that matters. In prey-specialists, venom is more potent
on particular types of prey (Michalek et al., 2019; Pekar et al., 2018).
Interestingly, previous studies have reported that spiders should
modulate venom release to avoid the considerable biochemical expense
of regenerating depleted reserves (Malli et al., 1998).
In a recent article (Michalek et al., 2019), adaptations of strictly
specialized and less specialized gnaphosid species were compared.
The behavioural approach as well as venom/silk glands size and
venom composition significantly differed between study species.
Smaller venom glands but larger piriform glands were found in lessspecialized
gnaphosid species (Michalek et al., 2019). The larger
venom glands in Drassodes might be linked to its being a generalist
species (Pekar et al., 2018), while the smaller venom glands in Zelotes
indicate a more specialized habit. So, it seems that the trade-off between
venom and silk materials is determined by the trophic strategy
rather than by the specimen's body size.
The comparative morphological analysis of ALS (PI and MA
glands) among some generalist ground spider representatives (Wolff
et al., 2017) points to another key element, the sticky silk, in the
evolution of araneophagy in ground spiders. The use of sticky silk
for prey immobilization is well-known from other araneophagous
web-building spiders, namely, cobweb spiders (Theridiidae) (Foelix,
1982). However, these have evolved an additional set of glands, the
aggregate glands, which produce viscid glue, and their ALS are not
modified (Coddington, 1989; Sahni et al., 2011). In gnaphosid spiders,
the piriform glands (PI) have diversified (Wolff et al., 2017),
which enables spiders to use sticky silk for effective prey immobilization.
A similar adaptation has also been observed in pholcid
spiders. Their piriform glands are enlarged (Huber, 2000), and this
modification may also be related to a special wrapping attack (Huber
& Fleckenstein, 2008; Jackson & Brassington, 1987). Despite the
modification of their ALS spinnerets, pholcids retain the ability to
spin attachment discs, but with modified shape. The modification
of ALS seems to be a universal adaptation in all ground spiders, no
matter whether they use venom or silk attack. This is supported by
the absence of a significant difference in the number of PI between
Drassodes and Zelotes.
In this article, we show the ability to shift attack behaviour in
two generalist ground spiders. Their behavioural adaptations are
highly plastic, enabling them to switch between strategies depending
on the type of prey. Behavioural observations also showed the
capture behaviour of Zelotes to be more stereotyped than that of
Drassodes; thus, we believe there is a degree of trophic adaptation
(preference in the use of attack strategies) in these spiders.
However, the linking of certain morphological characters (larger
venom glands in Drassodes and a smaller number of PI in Zelotes)
to behavioural adaptations was not supported. Thus, our results
suggest that behavioural adaptations are not paralleled with morphological
ones.
A C K N O W L E D G M E N T S
NB was supported by a grant from the International Visegrad
Fund (51910189 Act No. 40/1964), which allowed her to perform
a research stay in Czechia. MR was supported by a grant from the
Ministry of Education, Youth and Sports of the Czech Republic
(LTAUSA18171).
A U T H O R C O N T R I B U T I O N S
SP and NB conceived the study, designed the experiment, analysed
the data, and wrote the manuscript. MR performed the
morphological analysis and contributed to the writing of the
manuscript.
D A T A A V A I L A B I L I T Y S T A T E M E N T
The data that support the findings of this study are openly available
in [Depository of Terrestrial Invertebrate Research Group] at
[https://www.sci. muni.cz/zoolecol/inverteb/?page_id=18].
O R C I D
Narmin Beydizada https://orcid.org/0000-0002-2882-0292
Stano Pekar https://orcid.org/0000-0002-0197-5040
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How to cite this article: Beydizada, N., Řezáč, M., & Pekar, S.
(2022). Use of conditional prey attack strategies in two
generalist ground spider species. Ethology, 00,1-7. https://
doi.org/10.llll/eth.13268