Behavioral Ecology Vol. 12 No. 1: 1-7
© 2001 International Society for Behavioral Ecology
Decoy presentations as a means to manipulate the risk of extrapair copulation: an experimental study in a semicolonial raptor, the Montagu's harrier (Circus pygargus)
Centre d'Etudes Biologiques de Chizé, Centre National de la Recherche Scientifique, F-79360 Beauvoir sur Niort, France
Address correspondence to François Mougeot. E-mail: frm{at}ceh.ac.uk .
Received 23 March 1999; revised 23 July 1999; accepted 20 December 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Mate guarding and frequent copulations are two alternative paternity assurance strategies found in birds. In species with intense courtship feeding, like raptors, the "frequent copulation" strategy is expected because male food provisioning conflicts with mate guarding. We evaluated experimentally the paternity assurance behavior of a semicolonial raptor, the Montagu's harrier Circus pygargus, using decoy presentations to simulate territorial intrusions. Breeding pairs were exposed to male and female decoys at different periods during the female's reproductive cycle. Agonistic responses to decoys were intra-sexual, and the timing and intensity of male attacks toward male decoys supported responses related to the risk of extrapair copulation (EPC): Male aggression peaked during the presumed fertile period and almost disappeared after clutch completion. During the fertile period, copulation rate was significantly higher, and copulations lasted longer, during male decoy presentations than during controls. Males also spent more time close to the female during male decoy presentations compared to controls, both during the early prelaying and fertile periods, but not during incubation. In the fertile period, males also increased presence time close to the female in the hour following the removal of the male decoy. Conversely, female decoy presentations had no significant effect on copulatory behavior or male presence time. These results showed that the risk of EPC can be experimentally manipulated by the means of decoy presentations, simulating male territorial intrusions, and that male Montagu's harriers increase their short-term copulation frequency and female surveillance when they perceive themselves at an increased EPC risk.
Key words: Circus pygargus, copulation, experimental manipulation, mate guarding, sperm competition.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Cuckoldry has been documented in a wide range of bird species, and usually results from extrapair copulations (EPCs; Birkhead and Møller, 1992
; Westneat and Sherman,
1997). As cuckoldry decreases fitness of putative parents,
selection is expected to favor mechanisms that reduce its incidence
(Birkhead and Møller,
1992). Two main alternative paternity assurance strategies have
been so far described: mate guarding and frequent copulations. Mate guarding
is the commonest strategy, consisting of a close monitoring of the female
during the fertile period. The frequent copulations strategy ("Paternity
Assurance" hypothesis; Birkhead et
al., 1987; Møller and
Birkhead, 1992; Simmons,
1990) is based on sperm competition mechanisms (see
Birkhead and Parker, 1997), and
is particularly expected in birds that cannot guard their mates due to
ecological constraints (like in species with intense courtship feeding or in
colonially breeding birds; Birkhead and
Møller, 1992). However, high within-pair copulation
frequencies, even in nonguarding species, may not always be an indication of
sperm competition, as copulations may also serve functions other than
fertilization, like pair bonding or mate assessment (e.g.,
Tortosa and Redondo, 1992;
Villarroel et al., 1998). One
way of testing whether copulation frequency in a given species is related to
paternity assurance has been to look for differences in copulation rate in
situations of varying EPC risk, like breeding density (e.g.,
Arroyo, 1999;
Møller and Birkhead,
1993; Simmons,
1990; but see also Westneat
and Sherman, 1997). However, intraspecific studies of the
relationship between copulation rate and density should control for
potentially confounding variables. For instance, the risk of EPC may vary
between years according to breeding density, but may also differ according to
individual quality (e.g., Kempenaers et
al., 1992; Møller,
1998; Smith, 1988;
Wetton et al., 1995), and
individuals may choose not to breed close to others, depending on their
quality. For a given species, experimental manipulations may help to elucidate
whether a given behavior, like increased copulation frequency or mate
surveillance, appears as an individual response to a perceived EPC risk.
Experimental manipulations of individual EPC risk are rare; this has been done
only in passerines, by means of temporary male removals (e.g.,
Lifjeld et al., 1997) or
manipulation of male phenotype (e.g.,
Johnsen et al., 1998), which
is not feasible in all species. In this article, we investigated another
method to experimentally increase the risk of EPC and assess the paternity
assurance behaviors of a raptor species.
In raptors, males invest heavily in reproduction as they provide most of
the food for the female and the nestlings
(Newton, 1979). Cuckoldry
therefore potentially represents a high cost. Most species perform prelaying
courtship feeding, which conflicts with mate guarding, and copulate
frequently. Raptors are territorial, but some species are colonial
(Del Hoyo et al., 1994;
Newton, 1979), a situation
that may place males at a higher EPC risk (e.g.,
Arroyo, 1999;
Simmons, 1990). The Montagu's
harrier Circus pygargus is a semicolonial raptor with high male
parental investment. The species is socially monogamous, but EPCs have been
observed relatively frequently (ca. 6% of all copulations) and only in
colonial situations (Arroyo,
1999). Moreover, within-pair copulation frequency during the
laying period increased as the spacing between the nests used by breeding
pairs decreased, suggesting that copulation frequency is related to EPC risk
(Arroyo, 1999). In this study,
we used decoy presentations to simulate territorial intrusions and manipulate
experimentally the risk of EPC in Montagu's harriers. The sperm competition
hypothesis predicts that male territorial intrusions should peak when the
female is fertile, when EPCs can result in extra-pair fertilizations (EPFs;
Møller, 1987a). We set
up an experimental design according to this prediction: we presented pairs
with male and female decoys at different periods during the female's
reproductive cycle and expected male decoys presented during the fertile
period to be perceived as an increased EPC risk. This prediction was confirmed
by the timing and intensity of male agonistic responses. We then used this
experimental manipulation to investigate how males responded to an increased
EPC risk and precise the paternity assurance behaviors (mate guarding versus
frequent copulations) exhibited by the species.
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METHODS |
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Study species
The study was carried out in 1997-1998, in three 200-300 km2 study areas located in western France: (1) Marais de Rochefort (45°57' N, 0°55' W); (2) south of Deux Sèvres Department (46°11' N, 0°28' W), and (3) Baie de l'Aiguillon (46°24' N, 1°24' W). The populations of Montagu's harriers in these three areas have been monitored for four to 10 years, and each year all nests were located, and their breeding parameters monitored (see Arroyo et al., 1998
for more
details).
Female Montagu's harriers entirely rely on the food provisioned by the male
from the early prelaying until at least half of the chick rearing period, and
males contribute overall 80% of the food for the nestlings from hatching until
independence (Arroyo, 1995).
Male parental investment is thus high and EPF potentially represent an
important fitness cost. Montagu's harriers nest solitary or in loose colonies
(up to 27 pairs within 300 ha in our study areas;
Krogulec and Leroux, 1993) and
do not defend territories with fixed boundaries around the nest. Foraging
usually takes place away from the nesting areas, up to 7 km or even more
(Salamolard, 1997). For
simplicity, we define as "breeding territory" the area around the
nest site (ca. 50-150 m radius) where the female spends most of the time
between pair formation and laying. Mate choice takes place at arrival from the
winter quarters. The species is socially monogamous, but mate fidelity between
seasons is very low (<14%: Leroux and Bretagnolle, unpublished data), and
rare cases of polygyny and polyandry have been reported
(Cramp and Simmons, 1980;
Arroyo, 1996). Montagu's
harriers copulate at a low rate compared to other raptors (28-45 copulations
per clutch), but EPCs occur relatively frequently compared to other raptor
species (6% of copulations, n = 141) and in colonial situations
(Arroyo, 1999). Given the high
male parental investment, the semicolonial breeding and the occurrence of
EPCs, the Montagu's harrier is potentially a good model to study paternity
assurance behaviors.
Experimental procedure
We used Montagu's harrier plastic decoys to simulate territorial
intrusions. Pairs were presented with a male or a female decoy (the sexes are
highly dichromatic; Cramp and Simmons,
1980). Three experimental situations were tested: Presentation of
(1) female decoy; (2) male decoy with a prey (a dead mouse) at the feet, to
simulate a male delivering a prey; or (3) male decoy without prey. Each test
consisted of 2 h of continuous focal sampling of behavior: 1 h with
presentation of a decoy (experiment) preceded or followed, randomly, by 1 h
without decoy (control). By comparing male behavior during controls preceding
or following experiments, we may evaluate whether a perceived EPC risk still
affects male behavior once the decoy is removed (for instance, if female
surveillance persists after the territorial intrusion). The decoy was
presented on a pole and was always placed when the male was absent. In order
to minimize disturbance, the decoy was placed and removed quickly (in less
than 1 min). The observer was covered with a camouflage net while placing the
decoy if the female was present, and while removing the decoy. The birds never
alarmed while the decoy was placed or removed, but did so during nest visits,
so we believe that disturbance due to the observer was negligible. The
distance between decoy and nest site (25 to 100 m) was noted for each test.
Observations were then made from a hide or from a car. During experiments we
recorded: (1) detection time by the male, recorded when the male flew within a
50 m radius from the decoy, and approached it (either to inspect it, by close
circling, or to attack it); (2) male and female attack rate towards the decoy
(in attacks h-1, time being counted from detection). During both
controls and experiments, we also recorded (3) within-pair copulations, their
duration (in s) and their success (i.e., whether the male succeeded or not in
lowering its tail and achieving cloacal contact); (4) time spent by the male
within the breeding territory, and thus close to the female; and (5) male
display rate (display h-1, time being counted from detection).
A total of 93 tests were carried out on 45 different pairs. These were
selected from the 50-80 nests found each year, based on the presence of
recognizable individuals and the ease of conducting the experiments
(visibility, access). Study pairs included 18 (39%) wing-tagged males and 13
(28.3%) wing-tagged females. Additionally, 15 males and 16 females had
particular plumage features that allowed individual identification (double
black bar on wing, melanistic or dark plumage, advanced moult, broken
feathers, first-year birds). The remaining tests were conducted on isolated
pairs (without neighboring pairs within 2 km). Nests were visited once during
the incubation to check clutch size, and later in the season to measure and
band the chicks. Some nests were visited during laying, providing exact laying
dates: Eggs are laid on average each 2 days (1.5 to 3 days;
Cramp and Simmons, 1980) and
are blue, instead of white, for one day after laying
(Balfour, 1962;
Simmons, 1994). Otherwise,
laying onset was determined backdating from hatching date (see
Arroyo et al., 1998).
The onset of the female's fertile period depends on the length of time that
viable sperm can be stored by females
(Birkhead and Møller,
1992). Viable sperm storage duration is not known for Montagu's
harrier, but usually last 6-10 days in birds (e.g.,
Birkhead and Møller,
1992). In Montagu's harrier, within-pair copulation rate peaks
during the week preceding egg laying
(Arroyo, 1999, unpublished
data; Pandolfi et al., 1998),
indicating a peak in female's receptivity to copulations. Moreover, EPC
attempts and successful EPCs were observed only during the week before laying
and during laying (Arroyo,
1999, unpublished data). These observations suggest that female
Montagu's Harrier are fertile the week before laying. For the analyses, we
therefore classified tests a posteriori into three periods relative
to laying onset (day zero): (1) the days before -6 (from day -15 to -7),
hereafter referred as to the early prelaying period; females might have been
fertile during part of this period, but copulations occurring before day -6
probably had little chance to result in fertilization; (2) the days from day
-6 until the day before the last egg was laid (clutch size of study pairs
ranged from four to six eggs), hereafter referred as to the fertile period;
and (3) the incubation period (from the day the last egg was laid until
hatching).
Statistical analyses
Statistical analyses were performed on SAS 6.03
(SAS, 1988). Data were checked
for normality before performing parameteric tests, transformed if necessary
and, if still non-normally distributed, nonparametric statistics were used. We
used ANCOVA analyses to assess the effects of period, distance from the nest
and presence or not of prey on attack rate towards the decoys. For these
analyses, attack rate was log-transformed, so that it fitted a normal
distribution and its variance was homogeneous (Bartlett's test for homogeneity
of variances, p >.05). Male behavior (presence time, displaying
rate) was investigated by comparing experiments and their corresponding
control periods, using paired-sample tests. None or one copulation was usually
observed per control or experiment, the only exception being three consecutive
copulations (two unsuccessful followed by a successful one) during a male
decoy presentation in the fertile period. We transformed copulation frequency
into a binomial variable (occurrence versus. absence), and used logistic
regressions (Catmod procedure; SAS,
1988) to assess the effect of decoy presentations on copulation
probability. Each pair was tested on average twice (range one to four), but
only once with the same decoy for a given period. As the effects of decoy
presentations on presence time, display rate and copulation probability were
analyzed considering each period and decoy (male versus female) separately,
there was no pseudoreplication effect. However, it could affect our analyses
of detection time and attack rates, for which data from all periods were
pooled. We then analyzed the data (1) using all tests (71 male and 22 female
decoy presentations) and (2) using only the first test conducted on each pair
with each decoy (42 male and 18 female decoy presentations). Both analyses
gave the same results with regard to significance levels, so we present here
the results with the complete data set (n = 93).
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RESULTS |
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Decoy detection and attacks
The sex of the decoy had no effect on detection time by males (One-way ANOVA, F1,91 = 1.43, p =.24), nor did the distance between decoy and nest site (Linear regression, F1,91 = 1.16; p =.25). However, time to detection by males depended on period (F2,90 = 4.01, p =.021): it did not significantly differ between the early prelaying and fertile periods (16.3 ± 10.0 min, n = 32; and 18.6 ± 10.5 min, n = 44, respectively), but was significantly longer during the incubation period (27.4 ± 16.7 min, n = 17; Tukey tests, p <.05) when males visits were less frequent. Once detected, the decoy was usually attacked (83% of tests) by either the male, the female, or both. Males overall attacked male decoys significantly more frequently than their mates (Paired-samples t test: t70 = 5.70, p <.0001); this difference was significant during the early prelaying (Paired t test: t26 = 4.83, p <.001) and fertile periods (t32 = 6.09, p <.0001), but not during incubation period (t10 = 0.73, p =.48; Figure 1). The female decoy was overall attacked by females significantly more than by their mates (t21 = 2.60, p =.017; Figure 1). Intersexual attacks were thus rare and agonistic behavior towards decoys was mainly intrasexual.
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The average distance between decoy and nest site did not differ significantly between periods, whatever the decoy (One-way ANOVA: male decoy: F2,68 = 0.59, p =.56; female decoy: F2,19 = 0.11, p =.89). Male attack rate towards male decoys was significantly affected by the distance separating decoy and nest site, by the period the test was conducted and by their interaction, with no effect of adding a prey to the decoy (GLM; Period: F2,59 = 19.5, p <.0001; Distance, regressor: F1,59 = 3.69, p =.06; Prey: F1,59 = 0.62, p =.43; Period*Distance: F2,59 = 10.13, p <.001; all other interactions not significant). Males attacked the male decoy significantly more during the fertile period than during the early prelaying period, whereas they seldom attacked during the incubation period (Figure 1). Attack rate increased with decreasing distance between decoy and nest-site, although only during the fertile period (Figure 2a).
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In females, attack rate towards the female decoy did not differ significantly between periods (ANCOVA; F2,16 = 0.88, p =.43; Figure 1), but was affected by distance (F1,16 = 11.00, p =.004, Figure 2b), the interaction being not significant (F2,16 = 1.07, p =.37).
Effects of decoy presentations on male display rate
During the early prelaying period, male aerial display rate was not
significantly different during male decoy presentations (0.67 ± 0.84
display·h-1) and corresponding controls (0.41 ± 1.21
displays·h-1; Wilcox Matched-pairs Signed-rank test:
|Z| = 1.19, n = 27, p =.23). A significant
difference was however found during the fertile period (experiments: 1.22
± 1.51; controls: 0.27 ± 0.84 displays·h-1,
n = 33; |Z| = 3.50, p <.001). Male display
rate during experiments was not significantly different when the male decoy
was presented with or without a prey, whatever the period (Mann-Whitney U
test; early prelaying period: U = 79.5, p =.58, n =
27; fertile period: U = 132, p =.93, n = 33). A
female decoy presentation had no significant effect on male display rate,
whatever the period considered (early prelaying period: |Z| =
0.80, n = 5, p =.43 fertile period: |Z| =
1.34, n = 11, p =.18).
Effect of decoys on copulatory behavior
Copulation probability was not significantly different during controls and
female decoy presentations, whatever the period, nor was it during controls
and male decoy presentations during the early prelaying period
(Table 1). Conversely,
copulation probability was significantly affected by the presence of a male
decoy during the fertile period, being significantly higher during experiments
than during controls (Table 1,
Figure 3). Adding a prey to the
male decoy had no significant effect (Table
1) and copulation probability was not different during the
controls following or preceding male decoy presentations (Mann-Whitney U test:
early prelaying period: U = 79.5, p =.61; fertile period:
U = 120, p =.60).
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The success of a copulation depended on its duration (Logistic regression:
2 = 25.91, df = 1, p <.0001): all copulations
lasting 
2 s were unsuccessful, and all copulations lasting 
5 s were
successful. During the early prelaying period, the mean duration of
copulations was not significantly different between male decoy presentations
(4.5 ± 2.1 s, n = 6) and controls (4.0 ± 1.0 s,
n = 5: Mann-Whitney U test: U = 11, p
=.59). Copulation success was also similar during controls and experiments
(one out of five and one out of six unsuccessful copulations respectively;
Fisher's exact test: p =.81). During the fertile period, copulations
lasted significantly longer during male decoy presentations (5.7 ± 0.9
s, n = 18) than during controls (4.1 ± 0.7 s, n = 9;
U = 14, p =.002). However, similar proportions of
unsuccessful versus successful copulations were observed during controls and
male decoy presentations (one out of nine and two out of 18 respectively;
Fisher's exact test: p =.75). Mean copulation duration during
experiments was not significantly different when the male decoy was presented
with prey (5.5 ± 1.1 s, n = 10) or without prey (6.0 ±
0.8 s, n = 8; U = 29, p =.36).
Effect of decoys on male presence time
Males spent more time within the breeding territory during male decoy
presentations than controls at the early prelaying (Wilcox Matched-pairs
Signed-rank test: |Z| = 3.57, p =.004, n = 27)
and fertile periods (|Z| = 2.74, p =.006, n =
33), but no significant difference was found during the incubation period
(|Z| = 0.30, p =.76, n = 11). During the
fertile period, male presence time during controls was significantly longer
when the control was carried out after the test (male decoy presentations)
than when the control was before the test
(Figure 4, Mann-Whitney
U test: U = 79.5, p <.041, n = 33). No
such difference was found during the early prelaying period (U = 80,
p =.65, n = 27). The increase in male presence time was not
significantly different when the male decoy was presented with or without a
prey, whatever the period (early prelaying period: respectively + 18.1
± 20.0%, n = 12, and + 16.0 ± 18.9%, n = 15,
Mann-Whitney U test: U = 87.0, p =.90; fertile
period: respectively +9.6 ± 23.8%, n = 16 and +6.9 ±
26.7%, n = 17, U = 129.5, p =.82). A female decoy
presentation had no significant effect on male presence time, whatever the
period considered (early prelaying period: |Z| = 0.54,
p =.59, n = 5; fertile period: |Z| = 0.09,
p =.93, n = 11; incubation period: |Z| = 0.94,
p =.35, n = 6).
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DISCUSSION |
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Use of decoys as a tool for manipulating EPC risk
Birds can be easily lured by the means of decoys or stuffed animals, a method already used to study territorial (e.g., Gowaty, 1981
;
Wiklund and Village, 1992) or
anti-predator behavior (e.g., Dale et al.,
1996; Wiklund,
1990). In this study, we used decoy presentations to simulate
territorial intrusions and manipulate EPC risk. We first evaluate whether the
decoy was perceived as a conspecific. This was likely because: (1) agonistic
responses of Montagu's harriers towards decoys were intrasexual; (2) males
increased displaying rate in the presence of the decoy; (3) some females
solicited male decoys with prey; these three types of responses are unlikely
in interspecific contexts; (4) the same decoy painted as a carrion crow
Corvus corone (a local predator of harrier eggs), was attacked nine
times more intensively during the incubation period than when painted as a
conspecific and placed at the same distance from the nest (Arroyo, Mougeot and
Bretagnolle, unpublished data). We therefore consider that Montagu's harrier
perceived the decoys as conspecific intruders.
Second we evaluate whether male decoys were perceived as an increased EPC
risk. Agonistic responses supported intrasexual competition (see also
Wiklund and Village, 1992 for
similar results in the Eurasian kestrel Falco tinnunculus).
Intrasexual competition in males could result from either protection of nest
sites or food resources, competition for mates or paternity assurance
(Gowaty, 1981;
Møller, 1987a;
Wiklund and Village, 1992).
The Montagu's harrier is semicolonial, and typically does not defend food
resources associated with the nest site
(Salamolard, 1997). If
responses were related to nest site defense, the intensity of aggression would
either vary little over periods or decrease throughout prelaying
(Wiklund and Village, 1992).
Male agonistic responses related to competition for mates should peak early in
the prelaying period, when mate choice takes place or mate changes may occur.
Neither of these patterns was observed in male Montagu's harrier responses.
Moreover, in response to competition for mates, we would have expected an
effect of decoys on male displays in the early prelaying period rather than
during the fertile period. Aerial displays probably have agonistic as well as
sexual functions (Arroyo,
1995), and increased displaying rate during the fertile period may
therefore be another agonistic response to male decoy presentations.
Overall, temporal variation in the intensity of male agonistic behavior
(attacks, displays) best supported the hypothesis that male decoys were
perceived by males as an increased EPC risk: Intrasexual aggression was low in
the early prelaying period, peaked during the fertile period (when EPCs
occurred and when the risk of EPF is probably the greatest, see below), and
almost disappeared after laying was completed. The fact that a distance effect
in male attack rate was only found during the fertile period also suggests
that males responded to EPC risk, rather than territorially: The distance
between decoy and nest site is then equivalent to the distance between decoy
and female, which spends increasing time at nest. Similarly, in the Eurasian
kestrel, the distance over which males responded with overt aggression in
intrasexual contest decreased after clutch completion
(Wiklund and Village, 1992).
In other territorial birds, the size of the defended area also varies in
relation to paternity defense (e.g., barn swallows Hirundo rustica
and Yellowhammers Emberiza citrinella;
Møller, 1990).
The lack of intersexual aggression also supported the hypothesis that
intruding males represent an EPC risk: Most females (68%, n = 38)
never attacked and tolerated the presence of the male decoy. Furthermore,
three females, in the absence of their mate, landed close to the male decoy
presented with a prey and gave soliciting calls. These observations suggest
that some females solicit extra-pair males for food or for EPCs. Similar
observations were made in the Eurasian kestrel, in response to live decoys
(see Wiklund and Village,
1992). In Montagu's harrier, successful EPCs were almost always
solicited by the female (six out of seven EPCs), but were rarely traded
against prey (Arroyo, 1999,
unpublished data). The latter may explain why male aggression was not
different towards male decoys presented with or without prey. In conclusion,
agonistic responses supported the hypothesis that male decoy presentations
during the female's fertile period were perceived by males as an increased EPC
risk. We suggest that the use of decoys to manipulate EPC risk may also apply
for other species.
Conversely to males, the intensity of female intrasexual aggression,
although also depending on the distance between the female decoy and the nest
site, did not differ between periods. However, given the small number of
female decoy experiments conducted in this study, further investigations
should be carried out to conclude on the possible causes of female intrasexual
agonistic behavior (which may be related to competition for males, mate
guarding of male, nest defense, and/or to the risk of intraspecific brood
parasitism; Gowaty, 1981;
Wiklund and Village,
1992).
Paternity assurance behaviors in raptors
Frequent copulations
Most raptors copulate frequently and several authors have concluded that
sperm competition is the most likely cause of such high copulation rates
(e.g., Birkhead and Lessells,
1988; Koga and Shiraishi,
1994; Møller,
1987b; Negro et al.,
1992; Simmons,
1990; Sodhi,
1991). However, this has rarely been tested (see below) and
several species copulate frequently for other reasons than sperm competition,
like pair bonding and mate assessment (e.g.,
Negro et al. 1996;
Villarroel et al., 1998).
Given the fact that the exact duration of the fertile period is usually not
known, it is hard to tell which proportion of the copulations may serve in
pair bonding, mate assessment, fertilization or paternity assurance. Up to
now, the best support for paternity assurance through frequent copulations in
raptors came probably from empirical intraspecific comparisons: in several
species, copulation frequency increases with breeding density, a situation of
potentially increased EPC risk (Arroyo,
1999;
Korpimäki et
al., 1996; Simmons,
1990).
In this study, we showed that male Montagu's harriers increased their short
term copulation frequency in response to a male decoy presentation and during
the presumed female's fertile period, that is, when the risk of an EPC
becoming an EPF was potentially the greatest. Simulated male intrusions had no
significant effect on copulation frequency during the early prelaying period,
when copulations probably had little chance to result in fertilization. In
Montagu's harrier, EPCs attempts were observed only during the presumed
fertile period, and successful EPCs mainly during the laying period
(Arroyo, 1999, unpublished
data). The peak in within-pair copulation frequency prior to egg laying
(Arroyo, 1999, unpublished
data) might be a way for females to control paternity: Females may have
sufficient sperm from their partner to fertilize the clutch, and also retain
the option of engaging in an EPC if they encounter a more preferred male,
whose sperm will thus be favored (Birkhead
and Møller, 1993;
Birkhead and Parker, 1997).
However, males may counteract this risk by adjusting their copulatory behavior
during the female's fertile period and in situations where EPC risk is high;
females may have more interest in accepting than in rejecting within-pair
copulations, since they depend on their mate for food (see also
Korpimäki et
al., 1996). In birds, the last copulation before fertilization is
usually more successful than earlier ones, and the success of an EPC increases
with the interval between the previous pair copulation and the EPC
(Birkhead and Parker, 1997). By
copulating soon after discovering an extra-pair male near the female, male
Montagu's harrier may thus benefit from the last male fertilization advantage
(Birkhead and Møller,
1992; Birkhead and Parker,
1997) and reduce the risk that a possible EPC results in
fertilization.
During the fertile period, copulations performed during male decoy
presentations also lasted significantly longer than those performed during the
corresponding controls. Longer copulations may ensure copulation success
(i.e., the achievement of cloacal contact and sperm transfer) and may also
reflect increased sperm transfer to the female. Copulation success is probably
mainly under female control in the Montagu's harrier
(Pandolfi et al., 1998), as
well as in other raptor species (e.g.,
Birkhead and Lessells, 1988).
In this study, copulation success was overall high (82%, n = 11 and
89%, n = 27 copulations for the early prelaying and fertile periods,
respectively), and similar during controls and male decoy experiments. This
suggests that longer copulations might be related to increased sperm transfer,
which may be interesting for males in terms of sperm competition and
fertilization probability (Birkhead and
Møller, 1992; Birkhead
and Parker, 1997).
These experimental results show that individual male Montagu's harriers
adjust their short-term copulatory behavior when they perceive themselves at
an increased EPC risk; the results thus support the "Paternity
Assurance" hypothesis, and a frequent copulation paternity assurance
strategy in Montagu's Harrier. They are also consistent with and complementary
to empirical data, which showed that copulation rate during laying increased
with increasing breeding density (Arroyo,
1999). Copulation frequency was then likely to be adjusted to an
increased EPCs risk on colonies, which may be evaluated by the proximity of
other males, as well as more frequent male territorial intrusions in such
situations (Arroyo, 1995).
Female surveillance
We also found that male Montagu's harriers increased presence time within
their breeding territory and close to their female in response to male decoy
presentations, during both the early prelaying and fertile periods, but not
during the incubation period. This may be a by-product of male agonistic
behavior: males increased their presence time because they were occupied
attacking the intruder. However, during the fertile period, males did not only
increase presence time while the decoy was present, but also in the subsequent
hr. Males may have stayed after the experiment because of the disturbance (due
to the decoy or the observer). Such disturbance was, however, probably similar
for female decoy presentations, which did have no significant effect on male
presence time. Males may also have stayed if they needed to rest after
attacking the decoy; such behavior was, however, not observed during the early
prelaying period, nor after predator decoy presentations, which nevertheless
elicited a much higher frequency of attacks (Arroyo, Mougeot, and Bretagnolle,
unpublished data). Overall, female surveillance (mate guarding) was probably
the most likely explanation for the increase in male presence time after a
simulated male intrusion and during the fertile period.
Mate guarding is generally unexpected in birds with intense courtship
feeding because it conflicts with foraging: With males looking for food and
females staying near the nest site, the chances of maintaining an effective
surveillance of the female are reduced
(Birkhead and Møller,
1992; Møller,
1987b). However, male raptors may trade foraging and mate guarding
under certain circumstances, as suggested in other species (see
Birkhead and Lessells, 1988;
Korpimäki et
al., 1996; Simmons,
1990). Montagu's harriers breed and forage in open habitats, so
female surveillance might be possible at long distances (see also
Korpimäki et
al., 1996). Furthermore, males may change their hunting behavior
to increase surveillance, for instance foraging closer to their nest sites.
This may explain why decoys were detected more rapidly during the early
prelaying and fertile periods than during the incubation period. Nevertheless,
male Montagu's harriers still spent considerable time (ca. 50%) far from the
female during the critical fertile period, unlike mate guarding birds, which
spend >90% of their time following their female. Moreover, in some species,
males still loose paternity despite intense mate guarding (e.g.,
Johnsen et al., 1998;
Kempenaers et al., 1995).
Increased surveillance in Montagu's harrier therefore appears as the
"best-of-a-bad-job"
(Kempenaers et al., 1995): It
may help to see and repel some intruders, but it is probably not sufficient to
ensure paternity.
In conclusion, our experimental results support female surveillance during
the fertile period, despite the male courtship feeding strategy, as well as a
frequent copulation paternity assurance strategy in Montagu's Harriers. Mate
guarding and frequent copulation may thus be complementary means to ensure
paternity, as also suggested in some other courtship feeding raptors
(Birkhead and Lessells, 1988;
Korpimäki et
al., 1996). The former may help to detect and repel at least some
intruders, and reduce EPC opportunities, and the latter to minimize the risk
of EPCs becoming EPFs. A low incidence of EPF has been found in most raptors
so far studied, even in species with a high risk and occurrence of EPCs (e.g.,
Negro et al., 1996;
Swatschek et al., 1993;
Warkentin et al., 1994),
suggesting efficient paternity guards. In Montagu's harrier, paternity
analyzes have been performed in another population (eastern Poland) and
revealed no extra-pair fertilization
(Wiacek and Koziol, 1997).
Sample size was however small (eight pairs, 13 chicks;
Wiacek and Koziol, 1997), and
since EPF frequency may differ between populations of a given species (e.g.,
Petrie and Kempenaers, 1998),
paternity analyses should also be conducted in our study population to assess
whether male Montagu's harrier efficiently ensure paternity.
|
ACKNOWLEDGEMENTS |
|---|
We are grateful to A. Leroux, who initiated the wing-tagging program, and to A. Amar, R. Bernard, T. De Cornulier, T. Dieleveut, and M. Salamolard for their help in nest location and adult trapping. Part of the fieldwork was supported by a project of the Poitou Charente Region to V.B. and P. Duncan. We are also grateful to H. Fritz for statistical advice and to A.P. Møller and two anonymous referees for comments on the manuscript.
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REFERENCES |
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