A glimpse into the sexual biology of the ‘‘zygiellid’’ spider genus Leviellus
, and Matjazˇ Kuntner
Jovan Hadzˇi Institute
of Biology, Scientific Research Centre of the Slovenian Academy of Sciences and Arts, Novi trg 2, SI-1001 Ljubljana,
Slovenia. E-mail: firstname.lastname@example.org;
Department of Entomology, National Museum of Natural History,
Smithsonian Institution, Washington, DC, USA;
College of Life Sciences, Hubei University, Wuhan, Hubei, China
Abstract. We investigated the mating biology of the previously unstudied central European spider Leviellus thorelli
(Ausserer 1871) by staging laboratory mating trials using males and females of varying mating histories. Our aim was to
seek common themes in sexual behaviors of the sexually size-monomorphic ‘‘zygiellid’’ spiders with their putatively close
relatives, araneids and nephilids, which are relatively well studied with respect to sexual biology. We found L. thorelli
mating biology to more closely resemble that of sexually size-monomorphic araneids than that of dimorphic nephilids.
Unlike in nephilids with sexually conflicted adaptations, we found no evidence for genital damage or plugging in Leviellus
Wunderlich 2004, although we found rare cases of half-eunuchs. We suggest that the mating system of L. thorelli spiders is
determined by short female sexual attractiveness, reduced receptivity after mating and/or intensive mate guarding.
Keywords: Mating system, genital plugging, mate guarding, sexual-size dimorphism, eunuchs
Sexual conflict theory concerns the idea that males and
females may have different goals in reproduction (Watson 1991;
Chapman et al. 2003; Arnqvist & Rowe 2005). As a consequence
of intersexual conflict, various morphological, physiological and
behavioral adaptations have evolved, such as complex genitalia,
multiple sperm storage organs, toxicity of seminal fluids, sexual
cannibalism, and mate guarding (Parker 1984; Austad 1984;
Chapman et al. 1995; Kuntner et al. 2009a; Uhl et al. 2010).
These adaptations along with other demographic and ecological
factors shape the mating system of a species.
Among invertebrates, spiders represent an especially suitable
clade for sexual selection research (Eberhard 2004). In spiders,
the prevailing mating strategy may largely be determined by
two morphological constraints: genital morphology and
delayed female maturation. First, spiders are classified into
entelegyne and haplogyne species (Austad 1984; Uhl 2000; Uhl
et al. 2010; Kuntner et al. 2009a). Haplogyne species possess a
single insemination duct connected to spermathecae exhibiting
last-male sperm priority (Austad 1984; Uhl 2000; Uhl et al.
2010). Alternatively, the entelegyne spiders have separate
insemination and fertilization ducts connected to spermathecae
and overwhelmingly exhibit first-male sperm priority (Austad
1984; Uhl 2000; Uhl et al. 2010). As a consequence, males of
many entelegyne species have evolved mechanisms to avoid or
reduce sperm competition with rival males by pre- or post-
copulatory mate guarding and by the production of mating
plugs (reviewed in Uhl et al. 2010). Although these plugs are
thought to largely prevent or delay subsequent mating, they are
not universally effective even in closely related species, as
studies on nephilid spiders have shown [contrast e.g., Nephila
pilipes (Fabricius 1793), Nephilengys malabarensis (Walckenaer
1841) and Herennia multipuncta (Doleschall 1859)]: Fromhage
et al. 2007; Schneider et al. 2008; Kuntner et al. 2009b; Kralj-
Fisˇer et al. 2011). Besides mechanical plugging of stored sperm
and mate guarding, males employ other mechanisms to reduce
sperm competition. Such an example is chemical manipulation,
where products of male genitalia that are transferred during
copulation may induce female resistance for further matings or
earlier oviposition (Eberhard 1997).
Further behavioral and physiological adaptations also
shape the mating system of a given species. For example, in
highly dimorphic species that produce mating plugs, the small
males are often cannibalized after copulation (Nessler et al.
2009), either due to intersexual conflict (Arnqvist & Rowe
2005; Fromhage & Schneider 2005) or male sacrifice, which
may have a selective advantage in increasing paternity (Elgar
& Nash 1988; Andrade 1996; Elgar et al. 2000; Schneider et al.
2000) leading to monogynous mating systems. In some species,
males are physiologically limited to one mating (Downes 1978;
Michalik et al. 2010) or females are receptive to only one mate
(Alcock & Buchmann 1985).
Finally, female maturation in extremely sexually size
dimorphic species is usually considerably delayed (Higgins
2000; Kuntner & Coddington 2009; Kuntner et al. 2009b).
Along with ecological factors such as the duration of the
reproductive season, the operational sex ratio, the female or
male distribution and/or the travel costs to the mate (Riechert
1974, 1981; Fromhage et al. 2007, 2008), unsynchronized male
and female maturation may substantially constrain an
individual’s copulation frequency.
Clade-wide comparisons in mating behavior are essential
for revealing macroevolutionary patterns of mating strategies;
however, some groups remain largely understudied. Here, we
investigate a spider clade informally named ‘‘Zygiellidae’’,
which contains temperate and subtropical representatives of
several genera exhibiting a moderate sexual-size dimorphism,
but diverse entelegyne genital morphologies (M. Gregoric
unpublished data). Our ongoing phylogenetic work suggests a
close association of the ‘‘Zygiellidae’’ group with the families
Nephilidae and Araneidae. Within the former, sexual biology
has been well studied in many genera. Many exhibit extreme
sexual-size dimorphism and sexual cannibalism, where large
females devour tiny males (Kralj-Fisˇer et al. 2011). In
addition, males often engage in genital plugging, genital
damage and mate guarding (Schneider et al. 2008; Kuntner et
al. 2009a,b). In Araneidae, the sexual biology of most genera
remains unstudied, but with some notable exceptions, e.g.,
Argiope (Audouin 1826) with similar sexual phenomena as
2013. The Journal of Arachnology 41:387–391
found in Nephilidae (Fromhage et al. 2003; Foellmer &
Fairbairn 2004; Zimmer et al. 2012).
To investigate differences and similarities among the three
groups, we studied the sexual biology of a previously
unstudied ‘‘zygiellid’’ Leviellus thorelli (Ausserer 1871)
(Fig. 1). To determine whether the L. thorelli mating system
is monogamous or polygamous, we collected female and male
L. thorelli and tested them in staged mating experiments. We
measured spider body size to estimate the levels of sexual size
dimorphism (SSD), observed male-male competition and
determined the occurrence of plugging, genital damage and
Study animals.—Leviellus thorelli spiders were collected in
September and October 2009 on houses near Lukovica, central
Slovenia (46u099430N, 14u419300E). We collected 64 adult
spiders (33 females and 31 males) and kept them in the
laboratory for behavioral trials. We placed the collected
females into glass frames to allow them to build webs, whereas
males were kept in foam-covered plastic vials. We watered and
fed the spiders twice a week with Drosophila flies and
mealworms and maintained a seasonal light-dark cycle (16:8).
Experimental protocol.—In staged mating experiments in
the laboratory, we observed mating behavior and occurrences
of remating with the same genital organ. Mating was staged by
placing a male in the female web, approximately 10 cm away
from her. We observed male and female pre-copulatory
behavior (courtship), which palp (left/right/both) the male
inserted, how long and how many times the male inserted each
palp, which female copulatory opening (CO; left/right/both)
he inserted into, whether the spiders were aggressive and how
they behaved after copulation (e.g., mate guarding). Each
observation lasted for two hours. After a trial, we gave a
spider 1–12 days of rest before testing for remating.
To make inferences about the mating system, we conducted
four types of experimental trials, depending on female and
male mating history in the laboratory. We never staged a
mating trial between a male and a female that had been
previously tested together. In these trials we mated 1) both
sexes with unknown mating history [n545 trials, n564
spiders (28 individuals that did not mate in their first trial were
reused)], 2) previously copulated female and male with
unknown mating history (female remating, n510 trials), 3)
female with unknown mating history and a previously
copulated male (male remating, n58 trials), and 4) both
male and female previously copulated [female and male
remating, n58 trials (2 males used in Experiment 3 were
reused)]. When pairing already mated individuals, we devised
pairs in such a way that the male could insert his virgin palp
only into the female’s used CO (insertions were always
ipsilateral). For example, we paired a male with a virgin left
palp and a used right palp with a female with a used left CO
and a virgin right CO; hence, the virgin palp could be inserted
only in the used CO and vice versa. If remating did not occur
in two subsequent trials, we concluded that remating with the
used genital organ was not possible.
In three trials we placed two males on a female’s web to
document male-male antagonistic behavior. At the end of all
trials, the spiders were euthanized, fixed in 70%ethanol and
examined morphologically. Voucher specimens are available
from the authors.
Morphological examination.—We examined all specimens
from mating trials for genital damage (n564) and measured
their first tibia+patella lengths, carapace width and carapace
length (n550) under a Leica MZ16 stereomicroscope.
Following Kuntner & Coddington (2009), sexual-size dimor-
phism (SSD) is measured as the ratio of female to male body
length (or any other size measure).
We macerated all palps in concentrated KOH overnight in
order to make them transparent and expandable in distilled
water. We excised and examined all epigyna externally, then
macerated each epigynal preparation in concentrated KOH
overnight, and carefully cleaned it with needles in distilled
water (e.g., Kuntner et al. 2009b). This technique exposes the
dorsal epigynal anatomy and renders spermathecae translu-
cent, which allows any embolic leftovers lodged inside
spermathecae to be seen under a stereomicroscope.
Statistical analyses.—We examined the difference in body
size measures between the sexes using the Mann-Whitney U
Test. Correlations between size measures were analyzed using
the Pearson correlation. We used a Generalized Linear Mixed
Model (GLMM) to test the effect of two fixed factors, male
and female mating history in the laboratory (previously
unmated in the laboratory, previously mated in the laborato-
ry) and carapace length; and a random factor (individual code)
on occurrence of copulation (yes, no). We sequentially deleted
fixed terms in order of decreasing significance; only terms with
P#0.1 remained in the final model. We re-entered the
excluded terms one by one into the final model to confirm that
they did not explain a significant part of the variation. We ran
all analyses in PASW Statistics 18 (Field 2005).
SSD.—Patella +tibia I, carapace width and carapace
lengths were significantly correlated (patella +tibia I, carapace
width: r50.63, n550, P,0.001; patella +tibia I, carapace
Figure 1.—Female (A) and male (B) of the monomorphic Leviellus
thorelli. Scale bar 55 mm.
388 THE JOURNAL OF ARACHNOLOGY
length: r50.62, n550, P,0.001; carapace width, carapace
length r50.71, n550, P,0.001). The sexes differed
significantly in patella +tibia I length (Mann-Whitney U 591,
P,0.001, n550) but not in carapace length and width
(length: Mann-Whitney U 5254.5, P50.264, n550; width:
Mann-Whitney U 5231.5, P50.118, n550). Using carapace
length, SSD in L. thorelli was 1.29, which translates to a
sexually-size monomorphic species (Kuntner & Coddington
Mating results.—In all staged mating experiments (n571),
a male signaled a female by pulling or drumming on her web.
Typically, he initially remained at the edge of the female’s web
where he attached silk, created a mating thread, plucked the
threads of the female’s web with his front legs and rubbed his
palps. Eventually he walked on the mating thread toward the
female resting in her retreat and sometimes touched her legs
with his front legs. Then he retreated and rhythmically
plucked and beat the mating thread with his front legs. The
male repeated this sequence until the female emerged from her
retreat, if receptive. During courtship, the female usually
moved her first legs and palps and sometimes her abdomen,
and turned toward the male. When (if) the female joined the
male, they touched with legs in venter to venter position, then
suddenly grasped each other with legs to form a ball-shaped
outline (S1.—available online at http://www.bioone.org/doi/
suppl/10.1636/Hi13-08). The male inserted one of his palps
ipsilaterally. After approximately 7 min (mean 6SE, 6.82 6
1.35 min, n517) the female and the male abruptly separated,
the male usually hanging on the mating thread, and the female
retreating (S1). Then, the female typically rubbed her
copulatory openings with the third and fourth legs, whereas
the male positioned himself approximately 3–5 cm away from
the female, plucked the threads, and rubbed and cleaned his
palps. A male always continued to court after copulation, but
in no case did the pair copulate again. In most trials, the
female was not highly aggressive toward the male during or
after copulation, and sexual cannibalism was only observed
after one mating (5.9%). In some cases, however, the female
and the male were aggressive to each other before the
copulation, shaking the web and approaching each other with
open chelicerae. In such cases, mating never ensued.
If two males were introduced into the same female web, they
assumed an aggressive pose toward each other with front legs
extended, shook the web, fought vigorously and chased and
bit each other. In all three cases the larger male chased off the
smaller one (S2.—available online at http://www.bioone.org/
Of 71 mating trials (Fig. 2), copulation occurred in only 17
cases (23.9%). The occurrence of mating depended on male
and female mating history (F
541.81; P,0.001). The
male and the female copulated in 37.8%(n545) of the trials
when both of them had not previously copulated in our
experiments; however, we never observed spiders to copulate
in experiments 2, 3 and 4. That is, spiders never remated and
reused the genital organ they had previously used (n526
trials). The random effect was not significant.
Genital damage.—Two mated males (n517) emasculated
one palp to become half-eunuchs (Kuntner et al. 2009b) after
separating from the females they had copulated with. We
found the damaged palps in the males’ vials, implying that
they were not stuck in the female genitalia during copulation
but were rather self-removed after mating. Our morphological
examination revealed no further damage to male pedipalps (n
531) or any plug formation in female copulatory openings,
ducts or spermathecae (n533).
One of our goals was to look for common themes in sexual
behaviors of the sexual-size monomorphic ‘‘zygiellids’’ with
their close relatives, araneids and nephilids. Copulation
behavior of Leviellus thorelli resembles that of typical araneid
species; males construct and court on a mating thread, with
responsive females emerging out of the retreat and copulating
with the male in a ‘‘hug posture’’ on the mating thread
(Robinson 1982). Similar to other spiders with low levels of
SSD, male L. thorelli apparently do not damage their genitals
obligatorily and do not produce mating plugs, and females
exhibit low levels of sexual cannibalism. We found little
resemblance to nephilids, where extremely sexual-size dimor-
phic spiders engage in many ritualistic, sexually conflicted
behaviors and strategies (Kuntner 2005, 2006, 2007; Schneider
et al. 2005, 2008; Fromhage et al. 2007; Kuntner et al. 2009a,
b; Zhang et al. 2011). However, laboratory and field
observations of L. thorelli indicate intense mate guarding
probably due to first-male sperm priority, where males should
have reduced fitness benefits when mating with a previously
mated female (Austad 1984). Yet, the question of the mating
system in L. thorelli— and hence questions about macroevo-
lutionary patterns in mating strategies among the three
Among our aims was to determine the mating system in L.
thorelli. A male or a female that had previously copulated in
the laboratory was never observed remating, which could
suggest that both sexes in L. thorelli might be either
monogamous or at most bigamous. However, we acknowledge
here a serious limitation of our study, precluding such
definitive conclusion; we collected adult spiders from their
natural setting with unknown mating histories, whereas to be
conclusive, a study would better rear subadults to ensure
virginity. Despite these limitations, the fact is that we never
observed polygamy in L. thorelli, even though each individual
was tested at least twice, with two different potential mates.
Figure 2.—Copulation success in four different combinations of
female and male mating history in the laboratory. Unknown mating
history 5previously not mated in the lab.
ˇER ET AL.—LEVIELLUS MATING 389
Hence, (extreme) polygamy seems unlikely in the system
It is important to note that 60%of pairs failed to mate in
the staged experiments. We presume that those spiders had
mated before capture. If so, the females that received and
stored enough sperm might bias their energy investment in egg
production and fertilization, and hence might be sexually
unreceptive. It is also likely that females were only receptive
during molting and a short period thereafter (e.g., Alcock &
Buchmann 1985; Gaskett 2007). Mated or older spider females
can be aggressive and exhibit decreased receptivity to
subsequent courting males (Elgar 1998), e.g., Pholcus phalan-
gioides (Fuesslin 1775) (Scha¨fer & Uhl 2002), Argiope
keyserlingi Karsch 1878 (Herberstein et al. 2002) and
Tegenaria atrica C.L. Koch 1843 (Trabalon et al. 1997).
The alternative/additional explanation for the absence of
remating is that males do not find the mated females sexually
attractive, as is the case in Tegenaria atrica (Trabalon et al.
1997) and Agelenopsis aperta (Gertsch 1934) (Papke et al.
2001), both monogamous species that do not produce mating
plugs. Male spiders in general prefer virgin over mated
females, when females mate only once in several spiders;
e.g., Agelenopsis aperta (Riechert & Singer 1995). It may vary
among species whether a mated male or a female itself reduces
female attractiveness. One or more such mechanisms might
exist in L. thorelli, but this remains to be tested.
Based on our data, we cannot clarify why males did not
remate (with the used palp) with a newly introduced female.
Research on the closely related Zygiella x-notata indicates
male choosiness for mates (Bel-Venner et al. 2008; Venner
et al. 2010), where only 3%of guarding males switched to
another female (Bel-Venner & Venner 2006). Although
prolonged tandems during the reproductive season are known
to reduce sperm competition and to lower sexual harassment
of a mated female (Greenfield & Coffelt 1983; Scho¨fl &
Taborsky 2002), it would be worth studying if and what
mechanisms cause L. thorelli pairs to persist together in
nature, or even to remain monogamous after separation. A
phenomenon of prolonged tandems may relate to why no L.
thorelli males use both palps during mating. In the field and
laboratory, we observed that the male persists with the female
for a long period with recurrent courting phases. Hence, it is
possible that males use both palps with the same female, but
over a longer episode than the observed two-hour trial in the
Our results show no evidence for genital plugging, but we
recorded two cases of male L. thorelli becoming eunuchs by
severing their palps subsequent to mating. This resembles the
eunuch behavior of Herennia Thorell 1877 (Kuntner 2005;
Kuntner et al. 2009b), but not that of other nephilids where
males leave a palp in the female genital tract (Kuntner et al.
2009c; Kralj-Fisˇer et al. 2011; Li et al. 2012), nor that of
Tidarren Chamberlin & Ivie 1934 where the single-palped male
spontaneously dies while copulating and thus functions as a
whole-body mating plug (Knoflach & van Harten 2001).
Although the eunuch’s behavior in Leviellus is clearly not
obligate, it may nevertheless be suggestive of some level of
post-mating sterility in males.
In conclusion, L. thorelli sexual biology resembles that of
araneids with low SSD and not that of nephilids, which exhibit
pronounced SSD. Although our data require further corrob-
oration with lab-reared spiders, they suggest that the mating
system of L. thorelli spiders is shaped by a short period of
female sexual attractiveness and/or reduced receptivity after
mating and intensive mate guarding.
We thank Eva and Irena Kuntner and Cene Fisˇer for
logistic help, Jutta Schneider for comments on the early
manuscript version, and Martin Marzidovsˇek for making
available the video on male antagonism. This work was
funded by the Slovenian Research Agency (grant J12063 to M.
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Manuscript received 4 February 2013, revised 19 August 2013.
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