Factors influencing sexual cannibalism and its benefit to fecundity and offspring survival in the wolf spider Pardosa pseudoannulata (Araneae: Lycosidae)

Abstract

Sexual cannibalism is hypothesized to have evolved as a way to obtain a high-quality meal, as an extreme mate choice or as a consequence of female aggressive spillover. Here, we examined underlying factors likely to influence sexual cannibalism in the wolf spider Pardosa pseudoannulata (Bösenberg & Strand, 1906) from China, including mating status, female egg-laid status, female hunger level, female adult age and mate size dimorphism. The results showed that about 10 % of P. pseudoannulata virgin females cannibalized the approaching males before mating and that 28 % of P. pseudoannulata virgin females immediately cannibalized the males after mating. No incidents of sexual cannibalism during copulation were observed. Before mating, previously mated females and starved females tended to engage in significantly higher rates of attacks compared to virgin and well-fed females. Females that had laid egg sacs tended to engage in a significantly higher rate of attacks and sexual cannibalism than virgin females before mating. Regardless of pre- or post-mating, there was a strong positive relationship between mate size dimorphism and the occurrence of sexual cannibalism. We also tested the effects of sexual cannibalism on the fecundity of cannibalistic females and the survival of their offspring. Our results indicated that sexual cannibalism affected positively the offspring survival of cannibalistic females, but not fecundity. Our findings support the hypothesis that sexual cannibalism has evolved as an adaptive component of female foraging strategy and that it benefits offspring survival as a result of paternal investment. © 2012 Springer-Verlag Berlin Heidelberg.

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1 23
Behavioral Ecology and Sociobiology
ISSN 0340-5443
Volume 67
Number 2
Behav Ecol Sociobiol (2013) 67:205-212
DOI 10.1007/s00265-012-1440-2
Factors influencing sexual cannibalism
and its benefit to fecundity and offspring
survival in the wolf spider Pardosa
pseudoannulata (Araneae: Lycosidae)
Lingbing Wu, Huaping Zhang, Ting He,
Zeliang Liu & Yu Peng

1 23
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ORIGINAL PAPER
Factors influencing sexual cannibalism and its benefit
to fecundity and offspring survival in the wolf spider
Pardosa pseudoannulata (Araneae: Lycosidae)
Lingbing Wu &Huaping Zhang &Ting He &Zeliang Liu &Yu Peng
Received: 26 April 2012 /Revised: 6 October 2012 /Accepted: 12 October 2012 /Published online: 10 November 2012
#Springer-Verlag Berlin Heidelberg 2012
Abstract Sexual cannibalism is hypothesized to have evolved
as a way to obtain a high-quality meal, as an extreme mate
choice or as a consequence of female aggressive spillover.
Here, we examined underlying factors likely to influence sex-
ual cannibalism in the wolf spider Pardosa pseudoannulata
(Bösenberg & Strand, 1906) from China, including mating
status, female egg-laid status, female hunger level, female adult
age and mate size dimorphism. The results showed that about
10 % of P. pseudoannulata virgin females cannibalized the
approaching males before mating and that 28 % of P. p s e u -
doannulata virgin females immediately cannibalized the males
after mating. No incidents of sexual cannibalism during copu-
lation were observed. Before mating, previously mated females
and starved females tended to engage in significantly higher
rates of attacks compared to virgin and well-fed females.
Females that had laid egg sacs tended to engage in a signifi-
cantly higher rate of attacks and sexual cannibalism than virgin
females before mating. Regardless of pre- or post-mating, there
was a strong positive relationship between mate size dimor-
phism and the occurrence of sexual cannibalism. We also tested
the effects of sexual cannibalism on the fecundity of cannibal-
istic females and the survival of their offspring. Our results
indicated that sexual cannibalism affected positively the off-
spring survival of cannibalistic females, but not fecundity. Our
findings support the hypothesis that sexual cannibalism has
evolved as an adaptive component of female foraging strategy
and that it benefits offspring survival as a result of paternal
investment.
Keywords Araneae .Wolf spider .Pardosapseudoannulata .
Sexual cannibalism .Fecundity .Survival
Introduction
Sexual cannibalism, an extreme form of sexual conflict, is
defined as the killing and consumption of an actual or
potential mate by a female before, during, or after copu-
lation (Darwin 1871; Elgar 1992; Elgar and Schneider 2004;
Wilder and Rypstra 2008c; Wilder et al. 2009). Sexual
cannibalism has been observed in at least 30 species of
terrestrial arthropods, including members of all orders of
arachnids and three orders of insects (Polis 1981;Elgar
1992). Although present in a variety of taxa, sexual canni-
balism is relatively common in spiders and has been studied
most extensively in spiders (Buskirk et al. 1984; Elgar 1992;
Elgar and Schneider 2004; Wilder and Rypstra 2008c).
While sexual cannibalism is a relatively simple and un-
ambiguous behavior, the costs and benefits of sexual canni-
balism to males and females depend critically on whether it
occurs before or after insemination (Elgar 1992; Elgar and
Schneider 2004). Accordingly, the timing of sexual canni-
balism has profound implications for the extent to which the
behavior can be regarded as a male and/or female mating
strategy (Elgar and Schneider 2004). Pre-mating sexual
cannibalism entails extreme sexual conflict: males, who
must approach females in order to copulate, risk being killed
by the females they approach (Newman and Elgar 1991),
Communicated by M. Elgar
L. Wu :T. He :Z. Liu :Y. Peng (*)
College of Life Sciences, Hubei University,
Wuhan 430062, China
e-mail: hbdxpengyu@hotmail.com
H. Zhang
Yichang Agricultural Products
Safety Supervision and Inspection Station,
Yichang 443000, China
Present Address:
L. Wu
College of Life Sciences, Zhejiang University,
Hanzhou 310058, China
Behav Ecol Sociobiol (2013) 67:205–212
DOI 10.1007/s00265-012-1440-2
Author's personal copy

whereas females may acquire nutrient benefits by killing
and consuming approaching males instead of mating with
them (Schneider and Lubin 1998; Rabaneda-Bueno et al.
2008). When sexual cannibalism occurs before mating, it is
unambiguously not in the interest of the male, which forfeits
further reproductive efforts (Newman and Elgar 1991; Elgar
and Schneider 2004), while females may obtain nutritional
benefits although they also risk reproductive failure
(Schneider and Lubin 1998; Elgar and Schneider 2004). How-
ever, under other circumstances, post-mating sexual cannibal-
ism may be a strategy of either or both sexes (Buskirk et al.
1984; Elgar and Schneider 2004). A male may benefit from
post-mating sexual cannibalism through paternal investment
(Parker 1979; Buskirk et al. 1984)or/andmatingeffort
(Simmons and Parker 1989; Elgar and Schneider 2004;
Roggenbuck et al. 2011). Females gain nutrients that may
increase body mass (Elgar and Nash 1988;Elgar1998), body
condition (Barry et al. 2008), or fecundity (Birkhead et al.
1988;Johnson2001,2005; Barry et al. 2008).
Prior studies have demonstrated that some factors influ-
ence the occurrence of sexual cannibalism (Wise 2006;
Wilder and Rypstra 2008c; Roggenbuck et al. 2011). For
example, extensive observations of wolf spiders in the
field have revealed that rates of prey capture are very low
(Nyffeler and Benz 1988; Nyffeler and Breene 1990). Wise
(1993) showed that female spiders are generally food-
limited in the field and therefore should be motivated to
cannibalize males, especially if they have already mated
(Newman and Elgar 1991; Wise 2006; Wilder and Rypstra
2008c). Underlying factors that may influence the occur-
rence of sexual cannibalism deserve further attention and
include mating status (Rabaneda-Bueno et al. 2008), female
age (Persons and Uetz 2005), female hunger level (Wilder
and Rypstra 2008b; Roggenbuck et al. 2011) and sexual size
dimorphism (Wilder and Rypstra 2008c).
The entire phenomenon of sexual cannibalism and its ben-
efits may be important for both sexes (Welke and Schneider
2012). The foraging hypothesis is one of the most straightfor-
ward hypotheses: that the female can gain nutrients by killing
and consuming the male (Barry et al. 2009). However, the
evidence that sexual cannibalism evolved as an adaptive com-
ponent of female foraging strategies is equivocal (Elgar and
Schneider 2004). Some studies have documented fecundity
benefits for females through sexual cannibalism in praying
mantids (Birkhead et al. 1988; Barry et al. 2008) and in spiders
(Rabaneda-Bueno et al. 2008), whereas most studies have
failed to document fecundity benefits to females (Andrade
1996; Arnqvist and Henriksson 1997; Elgar et al. 2000;
Johnson 2001; Elgar and Schneider 2004). The potential
benefit for a male depends on the probability of whether his
contribution is advantageous to his own offspring or to the
offspring of rival males (Welke and Schneider 2012). The
benefit to males appears to be in the context of paternal
investment, and the male body as a paternal investment is
not a new proposal (Buskirk et al. 1984). A recent study of the
orb-web spider Argiope bruennichi demonstrated that sexual
cannibalism benefits offspring survival, in which cannibalistic
females produced offspring with a longer survival time than
the offspring of females that were prevented from eating males
(Welke and Schneider 2012).
The wolf spider Pardosa pseudoannulata from China is a
well-suited model for evaluating the underlying factors like-
ly to influence sexual cannibalism, and for testing whether
sexual cannibalism evolved as an adaptive component of
female foraging strategy. First, observations in nature and
field experiments reveal that female P. pseudoannulata can
exert sexual cannibalism (Zhao 1993). Second, field experi-
ments have established that predatory terrestrial arthropods
are frequently food- and nutrient-limited in nature (Wise
1993; Fagan et al. 2002; Denno and Fagan 2003; Fagan
and Denno 2004; Wise 2006). Extensive field observations
on wolf spiders have revealed that rates of prey capture are
very low (Nyffeler and Benz 1988; Nyffeler and Breene
1990) and that conspecifics may comprise up to 25 % of
the diet (Hallander 1970; Persons and Uetz 2005). Third,
adult P. pseudoannulata females are 1.3-fold times larger
than adult males, which may make males a potentially good
meal for females, especiallyincomparisonwithnatural
prey, which are on average several fold smaller. Moreover,
females are monandrous so the nutritional benefit of male
soma for female reproductive output will potentially benefit
the male as he will sire all of the offspring.
In the study reported here, we examined several under-
lying factors likely to affect the rates of sexual cannibalism
in the wolf spider P. pseudoannulata from China, including
female and male mating status, female egg-laid status,
female hunger level, female adult age and mate size dimor-
phism (female body length divided by male body length).
Since fecundity benefits for females through sexual canni-
balism have been found in the wolf spiders (Rabaneda-
Bueno et al. 2008), we hypothesized that sexual cannibalism
evolved as an adaptive component of female foraging strat-
egies. We first examined the rate of sexual cannibalism of P.
pseudoannulata. Then we tested the factors likely to affect
the rates of sexual cannibalism. Finally, we compared the
fecundity and offspring survival of cannibalistic females
with those of non-cannibalistic females.
Material and methods
Collection and rearing of the spiders
Pardosa pseudoannulata, a ground-dwelling spider widely
distributed in China, India, Korea, Japan and other countries
of East Asia (Song et al. 1999), is a medium-sized wolf
206 Behav Ecol Sociobiol (2013) 67:205–212
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spider (Lycosidae: Araneae) that occurs at high densities in
farm fields throughout China (Zhao 1993). Wolf spiders are
keen-sighted wandering spiders (Land 1985) that do not rely
on webs to capture food, but instead ambush or actively
pursue their prey. In most provinces of Central China, there
are two and a half generations of this species per year (Zhao
1993). P. pseudoannulata overwinters as a sub-adult or adult
in the soil or in the litter in natural habitats (Zhao 1993).
Their reproductive peaks occur in early May of the over-
wintering generation, in early July of the next generation
and in late September of the third generation (Zhao 1993).
The overwintering sub-adults and adults are inactive from
November to early March. Female wolf spiders carry the
egg sac attached to their spinnerets until the young emerge.
The emerging spiderlings climb onto the female’s abdomen,
where they remain for about 5 days until they disperse into
the leaf litter (Zhao 1993).
We collected 379 sub-adult males and females of P. p s e u -
doannulata during the day from farm fields of Maanshan
Forest Park, Wuhan (30°52′N, 114°31′E), Hubei Province,
China, in late June and early July 2011. The collected spiders
were kept individually and visually isolated from each other in
clear Plexiglas enclosures (length×width×height, 5.0×5.0×
7.5 cm) (SAIFU Inc., Ningbo, Zhejiang, China) under labora-
tory conditions, at 24±0.5 °C and 50–70 % relative humidity
(RH) and a 13:11-h (light:dark) photoperiod. Each spider was
fed 25–35 fruit flies (Drosophila melanogaster) twice per week
and had continual access to water in the form of a soaked cotton
wick inserted through a hole in the cage floor into a water-filled
reservoir below. Spiders matured in the laboratory (determined
by the completion of their final molt). The spiders used in the
trials were between 10 and 20 days of adult age, except in the
adult female age treatment. The adult females [mean ± standard
error of the mean (SEM) body length10.29±0.23 mm, range 9–
12 mm)] were larger than adult males (7.67± 0.04 mm, range
7–9mm).
Mating trials
Mating trials were conducted in plastic chambers (diame-
ter×height, 10.5× 12.0 cm) with smooth acetate walls. The
bottom of the arena was covered with a layer of plaster.
Between trials, we sprayed the arenas with 70 % ethanol and
rubbed the bottom of the arena to remove the top layer of
plaster and any chemical cues left from the previous trial.
Each arena was visually and seismically isolated from the
others by means of partitions and foamboard. Females were
introduced into the arenas and allowed to deposit phero-
mones and other chemical cues for 1 h before the male was
introduced. Trials began when the male was introduced and
ended 2 min after the end of mating (Wilder and Rypstra
2008a). Mating trials were abandoned if the female did not
display any attack or mating behavior within 30 min of the
male’s introduction into the arena. If sexual cannibalism
occurred, we allowed the female to consume the entire body
of the male. Because copulation duration in this species
varies from 19 to 93 min, we were able to record all mating
events, including courtship, attacks (before and after mat-
ing), and sexual cannibalism (before and after mating).
The effect of mating status and female egg-laid status
on sexual cannibalism
We randomly selected 87 pairs of virgin males and females for
mating trials. Before the trials, we recorded the body length of
87 pairs of virgin males and females to the nearest 0.01 mm,
using an ocular micrometer, and measured the mass of the
females to the nearest 0.1 mg. The mate size dimorphism was
measured as the ratio of female to male body length (female
body length divided by male body length). Females are larger
than males, and larger values of the ratio indicate a greater size
difference between males and females. After successful cop-
ulations (58/87), males and females were returned to their
original enclosures. Of the mated females, 32 females that
did not consume males were selected, and each was paired
with another randomly selected virgin male; another 26 mated
females were provided their original diet until they produced
an egg sac. Similarly, 28 mated males were selected, and each
was paired with another randomly selected virgin female.
Other mated individuals were released after the trials.
Thirty-three females with egg sacs were collected in early
July. After the spiderlings dispersed from the abdomen, the
females that had oviposited were kept separately in the
enclosures, as described above, and provided with 25–35
fruit flies (D. melanogaster). After an interval of 24 h, these
females were introduced into the arenas and allowed to
deposit pheromones and other chemical cues for 1 h before
a virgin male was introduced. Each female was randomly
paired with a virgin male for each trial.
The effect of female hunger level on sexual cannibalism
We performed two treatments. The diet of the females of the
control group was not changed after the final molt, and these
females were fed with 25–35 fruit flies twice per week (the
first experiment, 87 virgin males pairing with 87 virgin
females). Females in the hunger treatment (n015) were not
fed at all after their final molt. Females remained in the
feeding treatments for 10–14 days between maturation and
mating. Females of each group were individually paired
with a virgin male for mating trials. If the starved females
made no attempt to cannibalize the males before or after
mating, 15 fruit flies were offered directly to the females.
Females that also refused the alternative prey were assumed
not to be hungry and excluded from the final analysis
(Roggenbuck et al. 2011).
Behav Ecol Sociobiol (2013) 67:205–212 207
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The effect of female adult age on sexual cannibalism
Three groups of virgin females aged 1 day (n019), 10 days
(n014) or 20 days (n08), respectively, were used. Females
of each group were individually paired with a virgin male
for mating trials. We compared the different rates of sexual
cannibalism of the three groups.
The effects of sexual cannibalism on fecundity and offspring
survival
Following the mating trials, 26 mated females (16 cannibalistic
and 10 non-cannibalistic) were returned to their original clear
Plexiglas enclosures and maintained on their original diet until
they produced an egg sac. We recorded the day that the first egg
sac was produced and the total number of eggs for each egg
sac. We randomly selected ten egg sacs, and 20 second-instar
spiderlings from each egg sac of cannibalistic and non-
cannibalistic females for testing the effect of sexual cannibal-
ism on offspring survival. The spiderlings were kept individu-
ally in cylindrical glass cages (diameter 2 cm, height 12 cm)
with a layer of sponge (1.5 cm thick) moistened with water on
the bottom. The cages with spiders were kept in a chamber
maintained at 24± 0.5 °C and 50–70 % RH, under laboratory
conditions of a 13:11-h (light:dark) photoperiod. Each spider-
ling was fed with 5–15 fruit flies, and they were checked daily.
The number of dead spiderlings was recorded. Some spider-
lings escaped from their glass cages, and these were not includ-
ed in the final statistical analysis of the survival.
Statistical analysis
Binary logistic regression was used to predict pre- and post-
mating attack and sexual cannibalism based on male mating
status, female mating status, female oviposition status, female
hunger level, female age and mate size dimorphism. Rates of
attacks on males and cannibalism before versus after mating
were tested by the Pearson χ
2
test. The effect of sexual canni-
balism on fecundity in the females’first egg sacs was tested by
the generalize linear model (GLM), with sexual cannibalism
(cannibal or non-cannibal) as the fixed factor and female body
mass as the covariate. Kaplan–Meier survival analysis was used
to test the offspring survival. Statistical analyses were performed
with SPSS for Windows (ver. 14.0; SPSS Inc, Chicago, IL).
Results
The effect of mating status and female egg-laid status
on sexual cannibalism
Of the 87 virgin females paired with virgin males in the first
experiment, 58 (66.67 %) successfully mated. Copulation
duration in this species varied from 19 to 93 min, and the result
indicated that cannibalized malesinthisspeciessignificantly
increased copulation time (Mann–Whitney test: Z02.354, p0
0.019). Nineteen attacks occurred before mating (19/87) and 36
occurred after mating (36/58); the other ten mating trials were
abandoned because the respective female did not display any
attack or mating behavior within 30 min of introducing the
male into the chamber. Nine virgin females (9/87) engaged in
pre-mating sexual cannibalism, and 16 virgin females (16/58)
engaged in post-mating sexual cannibalism. The proportion of
females that engaged in attacks after mating was significantly
higher than that before mating (Pearson χ
2
test: χ
12
023.923,
p<0.001). Similarly, the proportion of females that engaged in
post-mating sexual cannibalism was significantly higher than
that of females which cannibalized before mating (Pearson χ
2
test: χ
12
07.250, p00.007) (Fig. 1). No instance of sexual
cannibalism in P. pseudoannulata during copulation was ob-
served. All males continued to court intensively, with the first
pair of legs beating the floor after being introduced into the
mating chamber, despite lunging responses and being chased
by the female. Most males were able to avoid sexual cannibal-
ism attempts and being chased by the female. When females
attempted cannibalism by lunging promptly, they caught and
killed the male. Nine of 19 attacks translated into sexual can-
nibalism before mating, and 16 of 36 attacks translated into
sexual cannibalism after mating. The results showed that there
was no difference in the male’s attempts to avoid cannibalism
between pre- and post-mating sexual cannibalism (Pearson χ
2
test: χ
12
00.043, p00.836). Moreover, there was a strong pos-
itive relationship between mate size dimorphism and the oc-
currence of attacks and sexual cannibalism regardless of pre- or
post-mating (Table 1).
Mating occurred in 71.43 % (20/28) of exposures of mated
males with virgin females (Table 2). Although most of the
males continued to court intensively after being introduced into
the mating chamber, none of the mated females and none of the
females that had oviposited succeeded in mating with virgin
males (Table 2). Previously mated females and females that had
oviposited tended to engage in significantly higher rates of
attacks compared to virgin females (Table 1). Females that
had oviposited were more likely to engage in pre-mating sexual
cannibalism (Table 1).There was no relationship between male
mating status and the occurrence of attacks and sexual canni-
balism regardless of pre- or post-mating (Table 1).
The effect of female hunger level on sexual cannibalism
About 46.67 % (7/15) of the females in the hunger treatment
mated. Before mating, starved females attacked males more
often than did well-fed females. However, starved females
and well-fed females engaged in post-mating attacks at
nearly equal rates, and there was no significant effect of
female hunger level on the rate of sexual cannibalism before
208 Behav Ecol Sociobiol (2013) 67:205–212
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mating as well as on the rate of sexual cannibalism after
mating (Table 1). The starved females, which did not can-
nibalize the males before or after mating, all promptly killed
15 fruit flies when these were offered.
The effect of female adult age on sexual cannibalism
Mating occurred in 31.58 % (6/19) of the females aged 1 day,
71.43 % (10/14) of the females aged 10 days and 75.00 % (6/8)
of the females aged 20 days exposed to virgin males. The
lower mating rate of the females aged 1 day might result
from the lower likelihood of mating of recently molted
females, because all males continued to intensively court
females aged 1 day after being introduced into the mating
chamber. There was no significant effect of female adult age
on the rate of attacks (pre-mating attacks, Pearson χ
2
test:
χ
22
02.130, p00.345; post-mating attacks, Pearson χ
2
test:
χ
22
01.564, p00.457) and sexual cannibalism (pre-mating
sexual cannibalism, Pearson χ
2
test: χ
22
00.436, p00.804;
post-mating sexual cannibalism, Pearson χ
2
test: χ
22
0
0.041, p00.980).
The effects of sexual cannibalism on fecundity and offspring
survival
We did not find any significant effect of sexual cannibalism on
fecundity in the females’first egg sacs. Cannibalistic females
did not have a shorter preoviposition period (Mann–Whitney
test: Z01.509, N
cannibal
0N
non-cannibal
023, p00.144). Females
did not benefit from consuming a single male by producing
significantly more offspring per egg sac (cannibalistic females,
mean ± SEM offspring084 ±11.77; non-cannibalistic females,
mean ± SEM offspring066±6.90) [analysis of covariance
(ANCOVA), F
1, 11
00.352, n022, p00.561]. Female body
mass had a significant effect on fecundity in the female’sfirst
egg sacs (ANCOVA, F
1, 11
06.814, n022, p00.018).
Survival of offspring produced by cannibalistic females
was significantly higher than that of offspring produced by
non-cannibalistic females (Kaplan–Meier analysis: log-rank
χ
12
043.335, n0268, p<0.001) (Fig. 2). The results indicat-
ed that 48.15 % (52/108) of the offspring produced by
cannibalistic females could survive longer than 30 days. In
contrast, only 11.88 % (19/160) of the offspring produced
by non-cannibalistic females could survive 30 days.
Discussion
Our results show that female mating status, female egg-laid
status and mate size dimorphism had significant effects on
sexual cannibalism in the wolf spider P. pseudoannulata.
There was no effect of male mating status, female hunger
level and female age on sexual cannibalism. Moreover,
females did not benefit from feeding on a male in terms of
breeding earlier or producing significantly more offspring
per egg sac; however, the survival of the offspring produced
by cannibalistic females was significantly higher than that of
the offspring produced by non-cannibalistic females.
Of the 87 virgin females paired with virgin males, the rate
of females that engaged in post-mating sexual cannibalism
was significantly higher than that of females engaging in pre-
mating cannibalism. This result may have been affected by the
design of the trials: the pairs of spiders were left together after
mating, which dramatically increased the opportunity for can-
nibalism. The rate of sexual cannibalism was not related to the
male mating status, but there was a significant effect of female
mating status on sexual cannibalism. Of the 28 mated males
0
5
10
15
20
25
30
35
pre-matin
g
post-matin
g
Rates of sexual cannibalisms (%)
Pearson 2 test
p = 0.007
n = 87 n = 58
Fig. 1 Comparison of the rate of pre-mating and post-mating sexual
cannibalism events. Numbers within the column indicate sample size
Table 1 Summary list of results
of binary logistic regression,
with variables and the effects on
pre- and post-mating attacks and
sexual cannibalism
*Significant effect at (p < 0.05)
Variables Pre-mating Post-mating
Attacks Cannibalism Attacks Cannibalism
χ
2
pχ
2
pχ
2
pχ
2
p
Male mating status 0.203 0.653 0.458 0.499 2.071 0.150 0.445 0.505
Mate size dimorphism 10.115 0.001* 10.331 0.001* 6.091 0.014* 10.231 0.002*
Female mating status 8.543 0.004* 0.140 0.708 ––
Female egg-laid status 11.205 0.001* 17.962 0.000* ––
Female hunger 12.808 0.000* 0.118 0.731 0.114 0.736 0.545 0.460
Behav Ecol Sociobiol (2013) 67:205–212 209
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tested, 20 mated with virgin females. In contrast, of the 32
mated females tested, none mated with virgin males and two
mated females cannibalized the approaching males, although
most of these males continued to court intensively with the
first pair of legs beating the floor despite lunging responses
and being chased by the female. In our previous report, P.
pseudoannulata was found to have a mating system in which
females are essentially monandrous, whereas males are po-
lygynous (Chen et al. 2009). Similar results were reported for
a North American wolf spider, Schizocosa ocreata (Norton
and Uetz 2005)andPardosa astrigera (Wu et al. 2008). In our
present study, previously mated females and females after
oviposition were more aggressive and more motivated to
attack than virgin females. A similar observation was reported
for Teg e n aria atr i c a by Trabalon et al. (1998). One possible
reason for this behavior is that P. pseudoannulata females can
store sufficient sperm and produce morethan one egg sac after
a successful copulation, reducing female motivation for
remating (Zhao 1993).
Contrary to our prediction, starved females of P. pseu-
doannulata were not more likely than well-fed females to
cannibalize a male. However, female motivation for sexual
cannibalism was positively influenced by female feeding
status. Starved females were more aggressive and engaged
in more pre-mating attacks than fed females. Similarly, in
the European garden spider Araneus diadematus, starved
females were found to be more likely than well-fed females
to attack the males (Roggenbuck et al. 2011). In a study on
the wolf spider Hogna helluo, Wilder and Rypstra (2008b)
found that experimentally food-limited females cannibalized
males more frequently than did well-fed females. Earlier
studies also showed that hunger is a significant predictor
of cannibalism (Andrade 1998; Lelito and Brown 2008).
These findings support the existence of a trade-off between
foraging and mating (Roggenbuck et al. 2011).
In the present study, mate size dimorphism influenced
sexual cannibalism irrespectively of the timing of mating.
Elgar and Nash (1988) found that sexual cannibalism in A.
diadematus was influenced by male body size, whereas
female body size had no influence on sexual cannibalism.
Size differences between mating males and females have a
strong effect on sexual cannibalism by influencing male
vulnerability to female aggression (Wilder and Rypstra
2008b). In the fishing spider Dolomedes fimbriatus, females
attack males of all sizes, but attack success varies with male
size (Arnqvist and Henriksson 1997; Roggenbuck et al.
2011). Wilder and Rypstra (2008c) were the first to suggest
that the degree of body size difference between males and
females was related to the phylogenetic distribution of sexual
cannibalism among a broad range of spiders. These authors
found a strong positive relationship between the average
sexual size dimorphism of a species and the frequency of
sexual cannibalism.
The evidence that sexual cannibalism evolved as an
adaptive component of female foraging strategy is equivo-
cal, and there is little evidence that the consumption of a
single male increases female fecundity in a broad range of
species (Elgar and Schneider 2004). Our finding that con-
suming a single male did not increase female fecundity is in
agreement with the results of a study on the Australian
redback spider by Andrade (1996). Fromhage et al. (2003)
reported no difference in the fecundity of females of the
highly sexually dimorphic Argiene bruennichi that did or
did not consume one or two males. Although some studies
have documented a higher fecundity of cannibals compared
to non-cannibals (Meffe and Crump 1987;Snyderetal.
Table 2 Frequencies of mating, pre- and post-mating attacks and sexual cannibalism with variables
Variables % Mating (n) Pre-mating Post-mating
% Attacks (n) % Cannibalism (n) % Attacks (n) % Cannibalism (n)
Male mating status 71.4 (20/28) 17.9 (5/28) 0 (0/28) 30.0 (6/20) 20.0 (4/20)
Female mating status 0 (0/32) 50.0 (16/32) 6.25 (2/32) ––
Female egg-laid status 0 (0/33) 54.5 (18/33) 48.5 (16/33) ––
Female hunger 46.7 (7/15) 40.0 (6/15) 13.3 (2/15) 28.6 (2/7) 14.3 (1/7)
0
20
40
60
80
100
0 5 10 15 20 25 30
Days
% survival
Cannibal Non-cannibal
Fig. 2 Comparison of survival of the offspring produced by cannibal-
istic females and non-cannibalistic females (Sample size: n0108 for
cannibals; n0160 for non-cannibals)
210 Behav Ecol Sociobiol (2013) 67:205–212
Author's personal copy

2000), other studies found a negative effect of cannibalism
on growth and reproduction (Mayntz and Toft 2006).
Arnqvist and Henriksson (1997) found little support for
the adaptive foraging hypothesis in the European fishing
spider D. fimbriatus. Our results do not support the hypoth-
esis that sexual cannibalism benefits female fecundity. One
potential explanation is that males may be a poor-quality
prey item. A study on the wolf spider H. helluo suggests that
males are prey of low nutritional value in comparison to
crickets, mainly because the body of the male spider con-
tains fewer lipids, which are essential for egg production
(Wilder and Rypstra 2010). Another explanation is that our
spiders were fed with D. melanogaster in the laboratory, and
the species or quality of prey may have differed from what
they capture in nature (Welke and Schneider 2012). This is
not a trivial issue, because increasing numbers of studies
reveal that differences in prey quality may affect the surviv-
al, growth and fecundity of predatory arthropods (Uetz
1992; Toft and Wise 1999; Mayntz and Toft 2001; Wilder
and Rypstra 2008a).
Sexually cannibalistic behavior may improve the female
reproductive success by increasing the fecundity and/or
survival of the cannibal (Elgar and Schneider 2004). There
is equivocal evidence for the former (Elgar and Schneider
2004), but better evidence for the latter (Welke and
Schneider 2012). Our results demonstrate that the survival
of offspring produced by cannibalistic females was signifi-
cantly higher than that of offspring produced by non-
cannibalistic females. Our findings do support the hypothe-
sis that sexual cannibalism evolves as an adaptive compo-
nent of female foraging strategy and that it benefits offspring
survival as a result of paternal investment. A recent
study in the orb-web spider A. bruennichi showed that
cannibalistic females produced offspring with a longer
survival time than the offspring of females that were
prevented from eating males (Welke and Schneider
2012). Facilitating sexual cannibalism may always be
the best strategy for a male because of the benefits of
increased paternity (Andrade 1996,1998). The signifi-
cantly higher survival rate found in our study may be
explained by the accumulation of essential substances
contained in the male sperm, or through an improved alloca-
tion of nutrients by cannibalistic females to their clutch (Welke
and Schneider 2012).
Acknowledgments This study was supported by the National
Natural Science Fund of China (31071895), the Natural Science Fund
of Hubei Province (2011CDB071) and the Key Scientific and Techno-
logical Projects of Wuhan (No: 201120722216–3). We are grateful to
the two anonymous reviewers and Professor Mark Elgar (the associate
editor) for suggestions and improvements to this manuscript. We also
thank Dr. Janet W. Reid (Biological consulting and editing services,
JWR Associates, New York, USA) for helping us edit the English for
the manuscript.
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