Do males of the great grey shrike, Lanius excubitor,
trade food for extrapair copulations?
PIOTR TRYJANOWSKI* & MARTIN HROMADA†
*Department of Avian Biology and Ecology, Adam Mickiewicz University
yDepartment of Zoology, University of South Bohemia
(Received 28 August 2003; initial acceptance 9 October 2003;
ﬁnal acceptance 17 June 2004; published online 11 November 2004; MS. number: 7835R)
In several animal species, males offer material gifts to females during a courtship or precopulatory display.
The provision of nutrients is a male investment that can increase female reproductive success; therefore
males can use such gifts to inﬂuence female choice. Clear examples of courtship feeding before extrapair
copulations are scarce, however. We investigated courtship feeding in the great grey shrike. Males offered
food both to their mate and to extrapair females. Food offered to extrapair females had a signiﬁcantly
higher energy value than that offered to the social mates. The size of prey offered may enable females to
judge a male’s quality. A larger gift resulted in a higher chance of copulation for males in both within- and
extrapair events. We conclude that the energy value of nuptial gifts can explain why females of some
species engage in extrapair copulations.
Ó2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Female animals often copulate with males that are not
their social partners; however, their motivation is still
a matter of discussion (Birkhead & Møller 1992; Grifﬁth &
Montgomerie 2003). Indirect genetic beneﬁts are thought
to be the most important reason for this behaviour (Petrie
& Kempenaers 1998); however, direct, or nongenetic,
reasons are most readily understood (Kondoh 2001;
Møller & Jennions 2001). Direct ﬁtness beneﬁts have been
equated with the material beneﬁts acquired by females,
and may derive from enhanced fertility, fecundity or
parental care obtained from mating with preferred males,
enhanced courtship feeding, higher quality of a breeding
territory, antipredator behaviour of a mate, or simply
the absence of directly transmitted diseases (Møller &
A male’s reproductive success is limited by the number
of females with which he copulates, whereas a female’s
reproductive success is limited by her investment in
offspring (Trivers 1972). Thus, in general, males can be
seen as the competing sex and females as the choosing sex
(Atmar 1991; Kondoh 2001).
A female’s choice of mate can be inﬂuenced by a male’s
investment of resources or time in courtship. Nongenetic
beneﬁts are an integral feature of the mating systems of
a variety of animals. Because the mating decision is
controlled primarily by females, males try to persuade
them by providing resources. Females prefer resources and
paternal ability that have a direct effect on their re-
productive success, and increase their fecundity (Møller
& Jennions 2001). There are many possible direct beneﬁts
and they have been recorded in many animal taxa,
including insects, ﬁsh, reptiles, birds and mammals. Such
nongenetic beneﬁts can comprise a territory with a crucial
resource (Cronin & Sherman 1977) or parental care (Smith
1979). Vigilant males, watching for predators, can also
allow females to spend more time foraging, collecting
food resources that will be needed to produce a clutch of
eggs (Artiss & Martin 1995).
The most common male investments in copulation are
those of a nutritional value, in the form of either male
secretions (Sakaluk 1984; Simmons 1990; Wedell 1993)or
prey items (Thornhill 1976; Stanford 1995), sometimes
even the male himself (Buskirk et al. 1984). None the less,
evidence of direct beneﬁts in extrapair copulations are
One of the species offering food is the great grey shrike,
a raptor-like passerine bird, in which the male gives prey
(rodents, birds, lizards, or large insects) to females
immediately before copulation (Yosef 1992; Lorek 1995).
The species breeds mainly solitarily in pairs 500–1000 m
from one another (Scho
¨n 1994a). However, cases of mixed
reproductive strategy, polygamy and even extrapair
Correspondence: P. Tryjanowski, Department of Avian Biology and
Ecology, Adam Mickiewicz University, Fredry 10, PL-61 701 Poznan
Poland (email: firstname.lastname@example.org). M. Hromada is at the
Department of Zoology, University of South Bohemia, Branis
31, CZ-370 05 C
˘jovice, Czech Republic.
0003–3472/04/$30.00/0 Ó2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
AN IM AL BEH AV IO U R, 2005, 69, 529–533
copulations have been recorded (Yosef 1992; Lorek 1995;
Shrikes are well known for impaling prey on thorns and
sharp sprigs. Yosef & Pinshow (1989) have shown in an
experimental study that great grey shrike females select
a mate according to the size of prey impaled, with larders
thus serving as an extended phenotype of a male. If the
amount of food stored by the males can drive female mate
choice, food provided before within and extrapair cop-
ulations by males may also inﬂuence the female’s decision
to copulate. Larger prey are likely to require a greater male
investment in terms of hunting time and energy. There-
fore, we hypothesized that the size of the nuptial gift
should reﬂect a male’s quality. We then predicted that
females should choose those males that provide them
with larger precopulatory food items because they would
gain both direct and potentially indirect beneﬁts. Conse-
quently, a male’s copulation success was predicted to be
related to the size of the nuptial gift.
The overall ﬁtness of a particular male can be elevated
by extrapair copulations, with a single extrapair event
representing a greater chance of fertilizing eggs than one
of many within-pair copulations (Birkhead & Møller
1992). There is good evidence that female choice in
extrapair copulations is based on male traits (Houtman
1992; Hasselquist et al. 1996). Therefore, assuming our
ﬁrst two hypotheses are correct, males should allocate
their courtship gifts strategically. If they actively seek
extrapair copulations, based on sexual selection theory,
they should offer larger prey to extrapair females.
The great grey shrike is a territorial, socially monoga-
mous bird. In the breeding season it defends large
territories covering ca. 20–50 ha (Scho
¨n 1994b). Pairs
produce a single brood each year, although replacement
clutches can occur after nest failures (Scho
¨n 1994a). Only
the female incubates, but young are fed and cared for by
both parents (Scho
¨n 1994a, b). Copulations are preceded
by precopulatory displays: the male faces the female,
shivers and ﬂutters his wings and utters a call or a quiet
song, and often offers a food gift (Carlson 1989; Lorek
1995). The courtship-feeding intensity culminates several
days before the ﬁrst egg is laid, when copulations are most
frequent (Lorek 1995).
We investigated the behaviour of the great grey shrike in
a high-density population (up to 24 breeding pairs/
) in western Poland, from the beginning of April
to mid-May in 1999–2002. Individuals were distinguished
by highly individual-speciﬁc wing patterns and eye-masks
¨n 1994c; Probst 2001), and some (6–14 in different
years) were individually marked with colour rings under
licence from the Ringing Center Department of Ornithol-
ogy, Polish Academy of Sciences (for more details on study
sites and methods see Lorek 1995; Tryjanowski et al.
1999). Twenty-two males with both intra- and extrapair
copulation attempts recorded were included in the study.
We considered a copulation attempt unsuccessful when
courtship display (postures, wing shivering or courtship
singing) by the male near the female (up to 0.5 m) was not
followed by copulation itself. Because it was not possible
to observe cloacal contact, we considered a copulation to
have occurred when the mating event lasted for 3 s or
more (Lorek 1995).
Data Analysis and Statistics
To determine whether nuptial gifts can indicate male
quality, we correlated the value of food items (represented
as energy content, see Table 1 and details below) delivered
before copulation in within-pair attempts with the food
value of items delivered in extrapair attempts, for partic-
ular males. To avoid pseudoreplication, we examined and
used in the analyses only one observation of a male
bringing food for each category.
To test whether males use larger prey items to solicit
extrapair copulations, we compared the energy content
(details below) of food items in within-pair and extra-pair
gifts of all males, using the Wilcoxon matched-pairs
We calculated the usable energy content of prey items
delivered as nuptial gifts from mean prey body size and
published values of gross energy (kJ/g) and metabolizable
energy coefﬁcient (the proportion of overall energy con-
tent of the food item for a particular food item; Karasov
1990; Myrcha & Pinowski 1970; Table 1). Daily energy
demand of the great grey shrike was estimated to be 113 kJ
in the Negev Desert, Israel (Degen et al. 1992).
To establish the importance of food delivered before
copulation, we compared the mean energy value of the
nuptial gift with that of food delivered to a fertile female
outside of copulation events. Female birds are thought to
be fertile until the laying of the penultimate egg (Birkhead
& Møller 1992). Female great grey shrikes, which lay up to
eight eggs and start incubation from the third egg, are
thus potentially fertile until the ﬁfth day of incubation
(Lorek 1995). Incubating females are fed almost exclusively
by their mates (our unpublished data, based on data
collected with digital cameras, from observations of 11
nests in the same study area), and thus males probably
provide a signiﬁcant part of the female’s energy require-
ments during the fertile period.
To determine the male’s investment in nuptial gifts, we
investigated handling times (s) necessary for catching and
processing the prey (including chasing, killing, transport
and dismemberment of prey). We observed 47 cases of
great grey shrikes hunting in the study area. Only
observations where we saw the full spectrum of foraging
behaviour (from resting time to hunt procedures) were
included in the analysis.
Statistical tests were performed according to Zar (1999)
and all tests are two tailed. Data are presented as
ANIMAL BEHAVIOUR, 69, 3
Males that offered courtship gifts of high energy value in
within-pair copulations also did so in extrapair events
(Spearman rank correlation: r
Z0.543, NZ17, PZ0.009).
The energy content of the nuptial gift in unsuccessful
copulation attempts (10.5 G15.1 kJ) was signiﬁcantly
lower than in successful attempts (76.8 G135.5 kJ) in
within-pair events (Mann–Whitney Utest: UZ129.5,
Z22, PZ0.029) and in extrapair events (un-
successful: 36.1 G45.2 kJ; successful: 277.1 G185.2 kJ;
Males offered different food items to extrapair females
than to their mates (Fig. 1). The mean energy content of
a gift offered to an extrapair female was nearly four times
higher (75.3 G56.3 kJ) than that for a male’s mate
(19.0 G39.0 kJ; NZ22 males that delivered food to both
an extrapair female and their mate; Wilcoxon matched-
pairs signed-ranks test; ZZ3.72, P!0.001). This repre-
sents 66.6 versus 16.8% of the female’s daily energy
requirement, respectively. The mean energy delivered
by a male to an incubating fertile female was
19.0 G30.2 kJ/h (16.8% of the female’s daily energy
requirement, NZ11 nests) and comprised an average of
one prey item/h.
The prey most frequently offered to extrapair females
(vertebrates) was more costly for males in terms of time
spent hunting. The handling time of hunting shrikes was
signiﬁcantly longer for vertebrate (33.0 G32.6 s) than for
invertebrate prey (5.5 G2.6 s; Wilcoxon matched-pairs
signed-ranks test: ZZ3.41, NZ16, P!0.001).
We have shown that the value of the courtship gift could
indicate a male’s quality. Males that offered larger prey to
their mate also did so when soliciting extrapair copula-
tions. Courtship gifts signalling the quality or rank of the
male have been recorded in a variety of animals, such as
hanging ﬂies, Hylobittacus apicalis, and chimpanzees, Pan
troglodytes (Alcock 1998). Great grey shrike males that were
able to offer larger (and more energy-rich) food items
before copulation were more often selected as sexual
partners. Female shrikes may choose the male before
copulation, just after the gift is delivered.
Copulation success of the males was signiﬁcantly higher
if they offered larger and more energy-rich prey. This was
true for both intrapair and extrapair copulations; no
extrapair copulations were successful without a gift pro-
Male great grey shrikes contributed considerably to the
nutrition of their mates during the fertile part of the
incubation period by providing a substantial proportion of
the female’s daily food requirement. This means that
males allocated their courtship gifts strategically to copu-
lation attempts that could improve their overall ﬁtness
more dramatically. This ﬁnding corresponds with the
predictions of sexual selection theory (Birkhead & Møller
Until recently, females were thought to gain only
indirect, genetic, beneﬁts from seeking extrapair copula-
tions (Petrie & Kempenaers 1998). Other examples of
direct beneﬁts to females from extrapair matings are scarce
in the literature. Female red-winged blackbirds, Agelaius
phoeniceus, primarily a polygamous bird, may gain in
terms of increased foraging opportunities on the territory
of her extrapair mate and from additional defence against
nest predators from this male if he is in a neighbouring
territory (Gray 1997). In the purple-throated humming-
bird, Eulampis jugularis, males provide cooperative females
with access to food sources in their territories, exchanging
food for copulation even during the nonbreeding season
(Wolf 1975). The only known example of similar behav-
iour in a socially monogamous species is the Ade
penguin, Pygoscelis adeliae, in which males exchange nest
material for copulations (Hunter & Davis 1998).
For males, seeking extrapair copulations is thought to be
a trade-off between investing in mate guarding and
parental care (Westneat et al. 1990). Nevertheless, in male
great grey shrikes the fertilization beneﬁts of precopulatory
Table 1. Energy content of food items offered by great grey shrike males to females before copulation
individual (g) GE (kJ/g)
individual (kJ) MEC
individual (kJ) DE (%) PR
Passer montanus 3.20 21.8 69.76 0.75 52.32 46.3 2.4
Microtus arvalis 4.20 23.5 98.77 0.75 74.08 65.6 1.5
Lacerta sp.0.83 22.1 18.26 0.75 13.69 12.1 8.2
Gryllus campestris 0.25 23.2 5.87 0.77 4.52 4.0 25.0
DM: Dry mass (our data and Myrcha & Pinowski 1970 for P. montanus): GE: gross energy, kJ/g dry mass (Karasov 1990); OE: overall energy
content (DM !GE); MEC: metabolizable energy coefﬁcient (Karasov 1990; we used a coefﬁcient of 0.75 for all vertebrates and the value for
G. domesticus for G. campestris); ME: metabolizable energy (OE !MEC); DE: % of bird’s daily energy requirement provided by one prey
individual (Degen et al. 1992); PR: number of prey required for bird’s daily energy requirement.
Number of prey items
Birds Voles Lizards Insects Without
Fig. 1. Number of nuptial gifts offered by males to females in within-
pair (,) and extrapair (-) copulations. Prey are shown by
taxonomic group. Gtest: G
TRYJANOWSHI & HROMADA: MALE SHRIKES BUY SEX 531
gift giving must be weighed against the costs of acquiring
such gifts. The capture of the larger vertebrate prey
required higher energy expenditure because the shrikes
had to chase them for longer than other prey. Furthermore,
if a male invests more time in hunting to obtain a suitable
nuptial gift for an extrapair copulation, he risks being
cuckolded himself. Whatever the risks, the tendency of
male shrikes to invest more in extrapair events suggests
some potential beneﬁts of this activity. We suggest that the
behaviour observed in male great grey shrikes reﬂects the
greater ﬁtness beneﬁts of a single successful extrapair event
than multiple within-pair copulations. The investment of
males in reproduction within a pair is high: they defend
a territory, participate in nest building, and feed and guard
their mates and offspring. By contrast, the only investment
in an extrapair copulation is food.
Direct beneﬁts for great grey shrike females were
obvious in our study. Possible genetic advantages should
be investigated further. If male ability to obtain valuable
prey is somehow heritable, females may gain both direct
and indirect beneﬁts by choosing the male that provides
them with the most valuable prey. However, mating with
extrapair males could be costly. Females of the lesser grey
shrike, Lanius minor, that engage in copulation with other
males are sometimes punished by males (Valera et al.
2003). The female could also be risking divorce and
a reduction in their partner’s investment (Valera et al.
2003). This may be why females have higher standards in
extrapair than within-pair copulations. Hence, the ob-
served pattern may arise from a balance between the costs
and beneﬁts of extrapair copulations to a female.
We investigated the possible motivation of male shrikes
for extrapair copulations. However, multiple mating by
female birds is also interesting. There is evidence that
mating with more than one partner is widespread in
females of many animal taxa, from insects to mammals
(Kondoh 2001). Material-beneﬁt polyandry, or prostitu-
tion polyandry (Alcock 1988), is the most readily un-
derstood of several hypotheses for multiple mating by
females. It states that both the females engaging in
multiple mating and the males providing the direct
beneﬁt play essential roles in the evolution of polyandry.
Therefore, the question arises: why has evidence for direct
beneﬁts in extrapair copulations been so scarce?
Future studies should investigate whether males that
invest more really can increase their chances of reproduc-
tive success through extrapair offspring. If not (which is
possible, see Valera et al. 2003), what exactly do both
extrapair partners obtain from sexual contact with each
We thank G. Lorek, M. Antczak, J. Grzybek, P. Czechowski,
P. Kaczorowski and P. T. Dolata for their ﬁeld assistance,
as well as P. Chylarecki, K. Halupka, I. Hromadova
P. F. Donald, F. Profﬁtt, P. Bellamy, T. H. Sparks, F. Sergio,
F. Valera, T. J. Valone and two anonymous referees for
helpful comments. R. Fuchs loaned us a video recorder
for the research. This research was funded by Adam
Mickiewicz University, Poznan
´, Poland, GEF/SGP Poland
grants and SGA grant of University of South Bohemia,
ˇjovice, Czech Republic. The ﬁnancial support
for data analyses was provided by a grant from the State
Committee for Scientiﬁc Research (6 PO 4F 04621).
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