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Animal behaviour

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The shield effect: nuptial gifts protect

males against pre-copulatory sexual
cannibalism

Research

Sren Toft1 and Maria J. Albo1,2

1

Cite this article: Toft S, Albo MJ. 2016 The

shield effect: nuptial gifts protect males
against pre-copulatory sexual cannibalism. Biol.
Lett. 12: 20151082.
http://dx.doi.org/10.1098/rsbl.2015.1082

Received: 5 January 2016

Accepted: 20 April 2016

Subject Areas:
behaviour
Keywords:
Araneae, counteradaptations, courtship,
sexual conflict, sexual selection

Author for correspondence:

Sren Toft
e-mail: soeren.toft@bios.au.dk

Electronic supplementary material is available

at http://dx.doi.org/10.1098/rsbl.2015.1082 or
via http://rsbl.royalsocietypublishing.org.

Department of Bioscience, Aarhus University, Aarhus 8000, Denmark

Laboratorio de Etologa, Ecologa y Evolucion, Instituto de Investigaciones Biologicas Clemente Estable,
Montevideo, Uruguay

ST, 0000-0002-2839-3921
Several not mutually exclusive functions have been ascribed to nuptial gifts
across different taxa. Although the idea that a nuptial prey gift may protect
the male from pre-copulatory sexual cannibalism is attractive, it has previously been considered of no importance based on indirect evidence and
rejected by experimental tests. We reinvestigated whether nuptial gifts
may function as a shield against female attacks during mating encounters
in the spider Pisaura mirabilis and whether female hunger influences the likelihood of cannibalistic attacks. The results showed that pre-copulatory
sexual cannibalism was enhanced when males courted without a gift and
this was independent of female hunger. We propose that the nuptial gift
trait has evolved partly as a counteradaptation to female aggression in
this spider species.

1. Introduction
Nuptial gift-giving behaviour has evolved independently in several forms
among invertebrate and vertebrate species, but often occurs as food gifts [13].
Explanations for the origin and maintenance of nutritional donations differ,
whether seen from the females or the males point of view. For females, any
package of nutrients obtained without extra costs will increase their fecundity
[1,4,5]. For males, nuptial gifts may function as paternal investment and/or
as mating effort, depending on whether the gift contributes to female/offspring
nutrition, and thus increases the number or quality of offspring, or if it serves
only for the male to obtain more matings [13]. These hypotheses include
the possibility that the male offers himself as the nuptial gift by promoting
sexual cannibalism [6,7]. A third hypothesis, applying to predatory and cannibalistic species, proposes that nuptial gifts may act as physical protection
against sexual cannibalism from aggressive females [8,9] but has so far received
no support [10 12].
For the spider Pisaura mirabilis, Bristowe [9, p. 187] noted that a male who
has been put in a females enclosure with no fly to offer her has been eaten himself, implying that carrying the gift in his chelicerae when approaching the
female might protect the male from a potentially cannibalistic attack. Such
attacks are known from near-natural [10] as well as laboratory settings. Because
of low frequency of sexual cannibalism (less than 5%) [11,13 15] the phenomenon was inferred to be an unimportant evolutionary force in this mating
system. However, a low cannibalism frequency may be owing to effective
male counteradaptations to avoid female aggression [15]. If the gift functions
in the way that Bristowe [9] imagined, experimentally removing the gift
should (all other things equal) expose the pre-adaptation risk of sexual

& 2016 The Author(s) Published by the Royal Society. All rights reserved.

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0.4

proportion cannibalistic

P
0.3

0.2
W
0.1
P+
W+
1

4
5
trial no.

Figure 1. Time-to-event curve showing the cumulative proportion of females

that had cannibalized a male partner during subsequent mating trials. Treatments: W, well-fed females staged with gift-carrying males; P, poorly
fed females staged with gift-carrying males; W2, well-fed females staged
with no-gift males; P2, poorly fed females staged with no-gift males. All
cases of sexual cannibalism in W2 and P2 treatments were pre-copulatory,
whereas the single one in P was post-copulatory. Statistical analysis in table 1.
stealing over all experiments with gift-carrying males did
not differ between hungry (P) and satiated (W) females
(x21 1:66, p 0.20).

2. Methods
Spiders were collected prior to their maturity moult. When
adult, the females were divided into a well-fed (W) and a
poorly fed (P) group. After 7 days, females from each group
were staged either with a gift-carrying () male or with a male
with no gift (2). The numbers of females in each group were:
nW 13; nW2 33; nP 15; nP2 46. We recorded the outcome as gift-stealing (i.e. females run away with the gift
without mating), cannibalism, mating or male rejection. Females
that did not cannibalize the male were tested again on the following days for up to 8 times. The results were analysed using
survival analysis (also known as time-to-event analysis): cox proportional hazards fit. For detailed description of methods see the
electronic supplementary material.

3. Results
The presence or absence of a gift was the most important
factor determining whether females cannibalized the males,
while feeding level had no significant influence (figure 1,
table 1). Poorly fed females were nearly twice as cannibalistic
as well-fed females, but this difference was not statistically
significant (table 1). Females staged with no-gift males were
on average more than six times as cannibalistic as females
staged with gift-carrying males. Of 79 females staged with
no-gift males, 15 (19%) cannibalized their partner, whereas
only one of 28 females (3.6%) cannibalized gift-carrying
males. All cases of sexual cannibalism committed against
no-gift males were pre-copulatory, whereas the single case
committed against a gift-carrying male was post-copulatory.
This happened in a P trial in direct continuation of a seemingly normal copulation. Cannibalism occurred in 15 of
280 tests (5.4%) with no-gift males, and in 13 of 200 tests
(6.5%) considering only the poorly fed females; thus the overall frequency of cannibalism per trial was 5.8%. One female in
W performed gift-stealing twice, and eight females in P
performed 10 cases of gift-stealing. The frequency of gift-

4. Discussion
The results confirmed the hypothesis that the nuptial gift in
P. mirabilis protects the male against pre-copulatory cannibalism. Possibly, our experimental design was more sensitive for
analysing infrequent events than that used in previous
studies. With the low frequency of cannibalism in all treatments, a very large sample size would be needed to
demonstrate a significant effect without repeated testing.
We believe this is the first experimental demonstration of
an anti-cannibalistic effect of a nuptial gift. We do not see
this as an alternative explanation for the evolution of giftgiving behaviour. Each of the mechanisms involved, i.e.
parental investment, mating effort and avoidance of sexual
cannibalism, may have enhanced the others synergistically
during the evolutionary process.
Most females of P. mirabilis were rather unaggressive
towards no-gift males even if they had starved for one or
even two weeks. Even after eight trials, only 30% of the
poorly fed females had cannibalized a no-gift suitor and
well-fed females even fewer (figure 1). The frequency of cannibalism against no-gift males was slightly elevated
compared with previous laboratory studies with gift-carrying
males. Precautions against a potentially lethal attack must be
important for males as soon as the risk is non-zero. Therefore,
a multitude of behavioural and morphological adaptations
have evolved to reduce this risk [25,26,28]. Sexual cannibalism can be considered the ultimate form of female mate
choice [6]. An elaborate courtship that informs the female
about the quality of the male [29] should also reduce the likelihood of a potentially cannibalistic attack. In many spiders,
particular courtship signals (visual, auditive, vibrational)
may serve this function [20,21]. In P. mirabilis, females trade
matings for food [30], and the presence of a nuptial gift is
the essential part of the courtship promoting female

Biol. Lett. 12: 20151082

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cannibalism. However, experiments with no-gift males either

did not find any sexual cannibalism [13] or at least reported
no increased frequency [1619].
Sexual cannibalism is a threat to males in many predatory
species including much of the order of spiders [6]. Male courtship partly serves to reduce female aggression and thus the
risk to the male of being cannibalized [20,21] or males may
choose to mate while the female is moulting [22]. It has also
been shown that the risk of sexual cannibalism in nongift-giving species (orb-web spiders, mantids) is reduced if
mating occurs while the female is feeding [2326]. Such evidence makes the nuptial gift a likely male anti-cannibalistic
strategy. In fact, Kuriwada & Kasuya [27] suggested that
nuptial gifts function as a protective male strategy also in
non-cannibalistic species where females are aggressive and
may harm males by biting and kicking. They empirically verified that in some crickets the nuptial gift (secretions from a
metanotal gland) protects the males from female aggression
and suggested that the hypothesis of a protective function of
the nuptial gift should be extended beyond sexual cannibalism
to include any courtship situations where female aggression is
costly to males. In this study, we reconsider whether male P.
mirabilis benefit from nuptial gifts as shields against sexual
cannibalism.

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Table 1. Cox proportional hazards test (likelihood ratio test) of cannibalistic events (n 107 females, 17 cannibalistic events, 90 censored values). The
dependent variable is the number of mating trials until the rst cannibalistic event of each female. W, well-fed females; P, poorly fed females.
95% CI

d.f.

x2

p-value

1.91
6.42

0.67 6.79
1.32 115.8

1
1

1.31
5.47

0.25
0.0193

0.54

0.46

feeding condition  gift

We conclude that pre-copulatory cannibalism and giftstealing are alternative behavioural options for aggressive
females, with gift-stealing being the most likely outcome if
the male has a gift, cannibalism if he has not. The low level
of sexual cannibalism in previous studies (and probably in
nature) is thus partly a result of low aggression in a majority
of the females, partly owing to male traits that may have
evolved as counteradaptations to female aggression. The
nuptial gift is one such counteradaptation, and we hypothesize that low sexual size dimorphism and strong forelegs
in males are others.

Ethics. The work conducted complies with the ethical regulations in

Denmark.
Data accessibility. The dataset supporting this article has been deposited
in Dryad: http://dx.doi.org/10.5061/dryad.q5m84.
Authors contributions. S.T. conceived, designed and performed the laboratory experiments, analysed the data and wrote the manuscript
draft. M.J.A. participated in the conception/design of the study
and in writing the manuscript. Both authors approved the final
version and agree to be accountable for all aspects of the work.

Competing interests. We have no competing interests.

Funding. S.T. was supported by a grant from the Carlsberg Foundation.
M.J.A. was supported by ANII (SNI), Uruguay.

Acknowledgement. We are indebted to three anonymous reviewers

whose comments improved the manuscript considerably.

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