Behavioral Ecology Vol. 12 No. 4: 412-418
© 2001 International Society for Behavioral Ecology
Do female pied flycatchers seek extrapair copulations with familiar males? A test of the incomplete knowledge hypothesis
a Department of Biology, University of Oslo, P.O. Box 1050 Blindern, N-0316 Oslo, Norway b Zoological Museum, University of Oslo, Sars gate 1, N-0562 Oslo, Norway
Address correspondence to T. Slagsvold. E-mail: tore.slagsvold{at}bio.uio.no .
Received 14 April 2000; revised 18 September 2000; accepted 27 September 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In birds with biparental care, great variation exists in the frequency of extrapair paternity. Several hypotheses have been proposed to account for this variation. We tested the incomplete knowledge hypothesis, which states that females are constrained in their knowledge of male quality and that this influences their willingness to engage in extrapair copulations (EPC). By selective removal and release of female pied flycatchers Ficedula hypoleuca, we created a situation where females finally settled with a social mate close to the site where a former social mate was breeding. According to the incomplete knowledge hypothesis, this would lower the threshold for females to seek extrapair copulations in cases where their former social mate was of higher quality than the one finally chosen. The hypothesis was not supported because manipulation of female settlement did not increase frequency of extrapair paternity, not even in cases where the female nested close to the previous mate and the current mate apparently was of lower quality because he was younger and more dull colored. However, we found that when extrapair paternity did occur, the cuckolder tended to be a familiar male (i.e., the female's initial social mate).
Key words: cuckoldry, extrapair paternity, Ficedula hypoleuca, pied flycatcher, polygamy.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In birds with biparental care, great variation exists in the frequency of extrapair paternity (EPP) between species, between different populations of a species, and within populations (e.g., Møller and Briskie, 1995
). This variation is poorly understood, and several hypotheses
have been proposed (Birkhead and
Møller, 1992; Gowaty,
1996; Petrie and Kempenaers,
1998). We tested the incomplete knowledge hypothesis
(Slagsvold and Lifjeld, 1997),
which states that females may be constrained during the period of mating, nest
building, and egg laying so that they have limited opportunity to assess the
quality of the various males present in the breeding area. It is assumed that
females control engagement in extrapair copulations (EPC) and that they are
only willing to perform EPCs when it is likely that the extrapair male is of
higher genetic quality than their own social mate. Some observations are
consistent with the hypothesis; in particular, the frequency of EPP often is
higher at high than at low breeding densities
(Westneat and Sherman, 1997).
However, this is only circumstantial evidence and experimental tests are
needed.
Here we report a study of occurrence of EPP in the pied flycatcher
Ficedula hypoleuca. The species is suitable for a test of the
incomplete knowledge hypothesis because females may be constrained in their
knowledge of male quality. This is because the species is migratory, nonsocial
outside the breeding season, site fidelity is low, and females arrive late in
the breeding season and only a short time before egg laying
(Lundberg and Alatalo, 1992).
Females spend from a few hours to a few days prospecting for a breeding site
and a mate, visiting only a limited number of males
(Dale and Slagsvold, 1996;
Dale et al., 1992;
Hovi and
Rätti, 1994). The frequency of EPP
is low (Brün
et al., 1996; Ellegren et al.,
1995; Lifjeld et al.,
1991; Rätti et al.,
1995,
2001; but see also
Gelter and
Tegelström, 1992). We asked whether
this is caused by constraints on female knowledge of male quality.
We manipulated female settlement so that females finally settled with a
social mate close to a site where their former social mate was breeding. The
focal female had been mated to the latter male earlier within the same
breeding season, but he became occupied by another female because of our
temporary removal of the focal female. We expected our manipulation to lower
the threshold for females to engage in EPCs because they now would have proper
knowledge of the quality of at least one potential extrapair mate. We assumed
that the focal female was able to find her former mate because female pied
flycatchers are able to identify and locate a male from his song even after
having been exposed to the song only for a short time
(Lampe and Slagsvold,
1998).
The following predictions were tested: (1) The level of EPP would be higher
for experimental than for control females. (2) In cases of EPP, the cuckolder
would primarily be the female's initial mate. (3) The level of EPP would be
negatively related to the distance between the nest of the previous and
current mate. This is because of increased costs of visiting and being visited
by males at longer distances as assumed by the hypothesis
(Slagsvold and Lifjeld, 1997).
(4) EPP would primarily occur when the initial mate was of higher genetic
quality than the final mate. The male characteristics that females use to
assess male genetic quality are unknown. Hence, we included several phenotypic
traits which at least seem to be of importance in female choice of social mate
(e.g., females prefer older males [Lifjeld
and Slagsvold, 1988], males that arrive at breeding sites early
[Alatalo et al., 1984;
Dale and Slagsvold, 1990],
males with bright plumage color
[Järvi et
al., 1987; Lifjeld and
Slagsvold, 1988; Sætre
et al., 1994], and males singing complex songs
[Lampe and Sætre,
1995]). (5) Local recruitment of young to the breeding population
may be higher from broods with EPP than from broods without EPP because in the
former cases the females may have succeeded in improving the quality of at
least some offspring.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study area and study species
The study was performed in a mixed deciduous—coniferous woodland area near Oslo, during spring in 1996-1998, under license from the Directorate for Nature Management in Norway. The study area covered about 55 ha and was provided with about 260 nest-boxes each year.
The pied flycatcher is a small, hole-nesting, insectivorous passerine bird
which usually is monogamous, but in which some 5-10% of the males may be
polygynous. The decision of female settlement seems to be made by the females,
not by the males (Dale and Slagsvold,
1994), and choice is based both on the quality of the nest site
(Alatalo et al., 1986;
Dale and Slagsvold, 1996;
Slagsvold, 1986) and the
quality of the male, including his display activity
(Slagsvold and Viljugrein,
1999), song quality (Lampe and
Sætre, 1995), plumage color
(Järvi et
al., 1987; Lifjeld and
Slagsvold, 1988; Sætre
et al., 1994), and mating status
(Dale and Slagsvold, 1996;
Slagsvold and Dale, 1994). The
species is single-brooded but may renest if the first nesting fails.
Females were removed after mating and released soon after the initial mate
had attracted a new female. This procedure was necessary because earlier
experiments showed that females tend to return and mate with the same male if
released within the same breeding season
(Slagsvold and Dale, 1991).
However, we have also shown that returning females have difficulty in
displacing a new female if the latter has been present for a day or more
(Dale and Slagsvold, 1995). In
such cases, the returning female tends to settle with another male in the
neighborhood (Slagsvold and Dale,
1991). Knowledge of this behavior formed the basis for the present
experiment.
Experimental females
We removed and then released 48 females; 18 disappeared, 5 settled with the
initial male, and 25 settled with a new male (final male) in the study area.
Of the latter females, two were excluded from the analysis because the
identity of the final social mate was uncertain, and one was excluded (but
included as a control; see below) because the initial mate had disappeared
when the female was released. We also included three females that switched
mate probably because of our trapping and handling. These females were never
removed, but they had the opportunity to obtain information on the quality of
the initial male. Hence, we were left with 25 females for the study (referred
to below as "experimental females"; 3 in 1996, 9 in 1997, and 13
in 1998). In three cases, the initial mate was the same for two different
focal females in the same year. All six females were included because they
settled with final males that differed in quality and in distances to the
nest-box of the initial male. One male was final male both in 1997 and 1998.
Both cases were accepted because the male differed in age and experience
between the two breeding seasons and because the initial males were different.
Focal females were only included once, except one female that was manipulated
both in 1997 and 1998. She was included because initial and final mates were
different in the two years.
Females were always removed before onset of egg laying, 0-13 days after having started nest building with the initial male (mean = 4.3, SD = 3.1, n = 25). The nest was also removed. The females were kept in captivity for 0-21 days (mean = 7.0, SD = 6.3, n = 25) and provided with mealworms and water. They were released close to their initial nest-box and started nest building with the final male 0-3 days after release (mean = 1.4, SD = 1.0, n = 25). Egg laying started 4-9 days after onset of nest building (mean = 5.9, SD = 1.4, n = 25), which was from 6 days before to 14 days after the onset of egg laying by the replacement female of the initial male (mean = 2.0, SD = 3.8, n = 25).
Control females
We analyzed paternity for 82 control nests, consisting of 3 groups. The
first group consisted of females that had been temporarily removed after
initial mating in the study area but that renested with the same male
(n = 5). In the second group, females that had started nest building
2-29 km away were kept in captivity and then released into the study area
(n = 31). These birds nested with a new male and they had no initial
mate present in the study area. We also included the case mentioned above
where a female had her first and repeat nesting attempt in the study area but
where the initial mate had disappeared. The third group consisted of females
that were never removed (n = 46). We excluded three cases where there
was a switch of social mate in the female's fertile period, probably caused by
predation of the first male from European sparrowhawk Accipiter
nisus.
Male characteristics and mating status
Soon after arrival, the males were color-ringed, and plumage color, ranging
from black and white (score 1) to brownish and femalelike (score 7;
Drost, 1936) was recorded. We
used half-scores in case of intermediate types, and mean values were used if
there were repeat measurements during the same year. Body mass was measured to
the nearest 0.1 g with a Pesola 50-g balance, and wing length was measured to
the nearest 0.5 mm using a flattened and straightened wing. Males were aged as
yearlings or older according to Karlsson et al.
(1986). We also have data on
the song of both mates for 18 of the experimental females. Song recordings
were done during the unmated stage (29 males), after female removal (4 males),
or in their secondary territory (3 males). Song repertoire size has been found
to be similar for individual males singing to attract a female in their first
and secondary territory (Lyngby,
1996). Songs were recorded using a Sony TC-D5 Pro(II) cassette
recorder with a Telinga II Pro parabolic microphone and headphones. The
recordings were analyzed using Canary 1.2.4 (Bioacoustic Research Program,
Cornell Laboratory of Ornithology). We measured song repertoire size as the
number of different song figures in 25 consecutive song strophes.
Daily visits to the nest-boxes made it possible to observe arrival and mating date of the males and date of onset of egg laying. Arrival time of males varied significantly between years, and values were standardized by using the deviation (in days) from the annual mean for the initial and final males involved. We applied a similar procedure for date of first mating. We classified females as monogamously mated or mated as primary or secondary female to a polygynous male. All nestlings were banded, which enabled a study of recruitment to the breeding population. We also visited the study area daily in the breeding season of 1999 and 2000 to search for recruits. We included recruits found in the study area (n = 14) and in other nest-box plots (n = 7). Distances between nest-boxes were log-transformed in statistical tests. Statistical tests are two-tailed.
Parentage analyses
A sample of 25-50 µl blood was taken by puncturing the brachial vein,
suspended in 1 ml Queens lysis buffer
(Seutin et al., 1991), and
stored in a refrigerator for later analysis. Blood was collected from the 25
experimental females, from their 127 chicks, and from their initial and final
social mates. We also collected blood from the 82 control families (426
chicks). For most males this was done soon after their arrival, for females in
the incubation period, and for chicks when about 6-9 days old.
DNA was extracted using the QIAamp blood kit (Qiagene). We analyzed
parentage by microsatellite typing, using five pied flycatcher markers
(FhU1-5; Ellegren, 1992;
Primmer et al., 1996) that
have been used successfully in previous studies of the species (e.g.,
Ellegren et al., 1995;
Lifjeld et al., 1997). Refer
to Ellegren et al. (1995) for
details of the polymerase chain reaction protocol. Allele frequencies,
calculated from the genotypes of all adults (separately for the 1996 sample
and 1997 and 1998 combined), were used to estimate the exclusion power of the
marker set (Jamieson 1994).
The combined exclusion probability was.998 and the probability of identity was
5 x 10-8, both for 1996 and for 1997 and 1998 combined.
Excluding the FhU1 marker only reduced the exclusion probability by.05%. Thus,
for the second half of the 1997 material and the complete 1998 material, we
only used the remaining four markers.
Probability of false inclusion was calculated according to Jeffreys et al.
(1992). Of the 553 analyzed
nestlings, 517 showed no mismatches with either parent and had a low mean
probability of chance inclusion (.0020 ±.0058 SD). One nestling showed
one paternal mismatch but had a relatively low probability of false inclusion
for the father after excluding the locus with the mismatch from the
calculations (.016). All these 518 nestlings are considered legitimate.
Thirty-one nestlings had 2 or more paternal mismatches, whereas they matched a
female allele in all loci, thus being sired by extrapair males. Two nestlings
had one paternal mismatch and a relatively high probability of chance
inclusion, excluding the mismatched locus (.020 and.043, respectively).
Furthermore, the mismatched alleles of these nestlings were the same size as
the ones of brood mates showing mismatches on other loci as well. We therefore
consider 33 nestlings to have resulted from EPCs. Two nestlings (both in 1998)
showed mismatches with both parents at two or more loci, and thus probably
resulting from egg dumping. These nestlings were excluded from all further
analyses. For 30 of the 33 extrapair young (EPY), a male present in the study
area matched the paternal genotype completely (mean probability of false
inclusion,.0026 ±.0041 SD).
Separated for the 3 years 1996-1998, the proportion of EPY was 6% (n = 328), 6% (n = 107), and 7% (n = 116), and the proportion of nests with EPY was 10% (n = 63), 9% (n = 22), and 14% (n = 22), respectively. Because there was no significant annual variation, we combined the data in the analyses below.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Frequency of EPP in experimental and control broods
EPP occurred in only 4 (16%) of the 25 broods where an experimental female finally mated with a male different from the one initially chosen and where the latter male was still present in the study area (1 in 1996, 1 in 1997, and 2 in 1998). The frequency of broods with EPP for the three control groups was 0% (n = 5) for females that returned to their initial mate after capture and release; 16% (n = 31) for females that had been kept in captivity but where the initial male was not present in the study area; and 4% (n = 46) for unmanipulated females. Hence, the frequency of broods with EPY was similar for experimental females (16%, n = 25) and for all control females combined (9%, n = 82;
2 = 0.49,
df = 1, p =.48) and similar for experimental females and for control
females kept in captivity (control groups 1 and 2 combined; 14%, n =
36; 2 = 0.02, df = 1, p =.89).
Identity of cuckolders
In two of the four experimental broods with EPP, four chicks were sired by
the initial mate and one chick by the final mate. In the two remaining cases
of EPP, the cuckolder was evidently not the initial mate. In the first case,
one chick was sired by the final male and one chick by a male that had his own
nest 360 m away. In the second case, two chicks were sired by the final male
and three chicks by an unknown male.
In the two cases of EPP where the initial male was the cuck-older, the distance between his final nest and the final nest of the focal female was 72 m and 203 m (Figure 1). Considering 203 m as a maximum distance for males to engage in EPC with the focal female, which may be a conservative value (see below), we found 10 and 13 males to defend nest-boxes within this range in the two cases of EPP (inital mates and unmated males included). In the two other cases of EPP, there were 10 and 12 males present within 203 m from the focal female's nest. If females engaged in EPC with a single random male within this range (203 m) from their nest, we can calculate the probability that they would have copulated by chance with their initial mate in each of four cases (p =.00006), in three of the four cases (p =.00263) and in two of the four cases (p =.04019). Combining these values, the probability that the four females would have copulated with two or more of the initial mates by chance would be only p =.043. The analysis is sensitive to the number of male neighbors included and so to the distance used (203 m). However, as mentioned above, cuckolders may have their own nest as much as 360 m away, and so a value of 203 m may be conservative.
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EPP and distance to initial mate
Initial mates remained in the same part of the study area when focal
females were removed and finally nested on average only 32 m (SD = 33, range
0-102, n = 25) away; in 11 cases using the same nest-box. The
distance between the site of the final nest of the focal female and the final
nest of her initial mate was, on average, 250 m (SD = 224, range 32-754,
n = 25; Figure 1). The
distance was slightly shorter in case of EPP than in case of no EPP
(Figure 1; mean values of 139
and 272 m), but this was not statistically significant (t = 0.79, df
= 23, p =.44).
EPP and male characteristics
Final mates arrived and became mated about a week later than initial mates
(Table 1). The plumage color of
final mates tended to be slightly more brownish than that of initial mates but
not significantly so (Table 1).
Mean song repertoire size was similar for the two groups of males, as was mean
wing length and body mass (Table
1). In 16 cases, both males belonged to the same age class (14
older, 2 yearlings); in 7 cases the final male was yearling and the initial
male older; and in 2 cases the final male was older and the initial male was
yearling.
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Our manipulation did not necessarily result in great average differences in characteristics between intial and final males (Table 1); however, it resulted in great changes of mate characteristics for individual females between first and repeat nesting attempts. For instance, in one case the plumage color score was 2.5 and 5.5 for the initial and final male, whereas in another case scores were 5.5 and 3.0, respectively (Figure 2). The female that chose the initial male with the largest song repertoire of all the males analyzed (65 song figures) ended up with a final mate with one of the smallest song repertoires (17 song figures; Figure 3). In total, in 15 of 25 (60%) final mates were duller in color than the respective initial mates (Figure 2), and 7 of 18 (39%) had a smaller song repertoire (Figure 3). However, neither male color nor song repertoire size seemed to influence the rate of EPP because cuckolded final males were not more brownish, nor did they have smaller repertoires than the respective initial males (Figure 2 and 3). Moreover, the cuckolded final males were not more brownish, nor did they have smaller song repertoires than noncuckolded final males (Table 1). It should be noted, however, that the power of the latter tests were low due to few cases of EPP. Only four females settled with final mates that were both duller and had less complex song than the first mate; one of these females engaged in EPC with her initial mate.
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There was no significant correlation between color score of first and final mates (r =.12, n = 25, p =.56), nor of song repertoire size of first and final mates (r = -.15, n = 18, p =.55), and hence no evidence for consistent female preferences with respect to male plumage color or song repertoires.
For the experimental group, there was no significant difference between cuckolded and noncuckolded males in wing length, body mass, arrival date, mating date, and interval between arrival and mating (Table 1). In the two cases of EPP where the initial male was the cuckolder, the final male was a yearling in one case and an older male in the other case. The same was true for the two cases of EPP where identity of the cuckolder was unknown. In all four cases of EPP the intial male was older. Of the noncuckolded final males, 7 were yearlings and 14 were older.
Shortest distance recorded between final nest of experimental females and nest of initial mate was only 32 m (Figure 1). In that case, the final male arrived late (10 June), was a yearling, and was brown (score 6). The initial male arrived much earlier (25 May), nested in the study area in a previous year, and was much darker in color (score 3.2). The focal female had spent 6 days with the initial male before our removal. Nevertheless, the final social mate sired all her four chicks. The initial mate sired all five chicks in his own nest, where egg laying had started 6 days earlier than in the nest of the focal female.
Other patterns of EPP
Occurrence of EPP was unrelated to the egg-laying interval between the two
females (Figure 1; t =
0.02, df = 23, p =.98). In the two cases where the initial mate was
the cuckolder, the time elapsing from removal of the focal female from the
initial mate to her onset of egg laying was 7 and 14 days, respectively.
There was a tendency that fewer experimental females (24%, n = 25)
were mated with a polygynous male than controls (48%, n = 82;
2 = 3.45, df = 1, p =.063). However, the frequency of
EPP was almost the same for females mated with monogamous (10%, n =
62) and polygynous (11%, n = 45) males (2 = 0.01, df
= 1, p =.94).
EPP and recruitment
Of the nestlings reared in 1996-1998 later found as yearlings or older, 8
were offspring of experimental females (6.7% of young fledged, n =
119) and 13 were offspring of controls (3.5% of young fledged, n =
371); 1 was from a brood with EPP (2.0% of young fledged, n = 51),
and 20 were from broods without EPP (4.6% of young fledged, n = 439).
If we only include broods that produced at least one chick fledged, mean
number of recruits per brood was insignificantly higher for experimental
females (0.33, SD = 0.76, n = 24) than for controls (0.18, SD = 0.42,
n = 72; t = 1.23, df = 94, p =.22) and
insignificantly lower for broods with EPP (0.09, SD = 0.30, n = 11)
than for broods without EPP (0.24, SD = 0.55, n = 84; t =
0.85, df = 94, p =.40). The recruit from the brood with EPP was sired
by an EPC.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We assumed that female pied flycatchers have restricted knowledge of male quality. This assumption was based on the fact that females are migratory and spend only a few hours or days prospecting for a breeding site and a mate, visiting only a few males (Dale and Slagsvold, 1996
; Dale et al.,
1992; Hovi and
Rätti, 1994). In an earlier
experiment with the same population, we found that 28% of the females visited
only a single male before settling; mean number of males visited was 3.1
(Dale and Slagsvold, 1996).
This rapid settlement is caused by late arrival to the breeding ground and a
short breeding season and also by strong competition for nest sites. Females
restrict the extent of mate search if they encounter many prospecting females
(Dale et al., 1992). Males also
compete strongly for access to suitable nest sites, and this competition is
primarily related to time of occupancy and less to male characteristics
(Alatalo et al., 1986;
Slagsvold, 1986). However,
males with more complex songs tend to occupy more popular territories, and
they also tend to be mated earlier than males with less complex songs (Lampe
and Espmark, in press). In general, early-arriving males tend to be of higher
quality (i.e., they are older, in better condition, have brighter plumage
color, and have more complex songs; Lampe
and Espmark, 1994). They potentially have the chance to occupy the
best territories. However, a male occupying a good nest site may not always be
of preferred genetic quality, and thus females may be expected to adjust
initial mate choice by engaging in EPC
(Birkhead and Møoller,
1992).
We found that the frequency of broods with EPP was not significantly higher
for experimental females (16%, n = 25) than for controls (10%,
n = 82). The level of EPP was also similar to what we have found for
the same population in two earlier breeding seasons: 15% (n = 27) in
1989 (Lifjeld et al., 1991)
and 17% (n = 18) in 1992
(Ellegren et al., 1995). In
the present study, we manipulated female settlement so that a familiar male
was present in the neighborhood. However, females apparently did not take
advantage of this by increasing the level of EPP, even when their final social
mate appeared to be of much lower phenotypic quality than their initial mate.
This lends little support to prediction 1 (see Introduction) from the
incomplete knowledge hypothesis. The prediction is based on the assumption
that the addressed aspects of male phenotype could be used by females to
assess male genetic quality. This assumption was not tested, but
circumstantial evidence comes from the fact that male plumage color is partly
heritable in pied flycatchers (Lundberg
and Alatalo, 1992; Slagsvold
and Lifjeld, 1992). The frequency of EPP was so low that
prediction 3 on a relationship with distances between initial and finale mate,
and prediction 4 on a relationship with quality differences between the two
mates, could not be critically tested. Support was only found for prediction 2
because, when EPP occurred, the cuckolder tended to be a familiar male.
We conclude that the low frequency of EPP in this species does not seem to
be explained by females having incomplete knowledge of male quality. It may be
argued that the initial males were located too far away from focal females to
be visited (e.g., because of risk of predation from European sparrowhawks;
Slagsvold and Dale, 1996).
This possibility can be rejected because distances between nest-boxes of
initial and final mates were low in many cases
(Figure 1). Moreover, initial
mates remained in the same area when focal females were removed, so focal
females presumably would have no difficulty locating their former mates. On
the other hand, the initial mate's new female may not have tolerated intrusion
by the experimental females, thus preventing these females in engaging in EPCs
with their former mate. Female pied flycatchers have been shown to be very
aggressive toward other females close to the nest site and also toward
prospecting females in the mate's second territory
(Slagsvold and Sætre,
1991; Slagsvold et al.,
1992;
Rätti,
1999). Hence, it is perhaps more likely that resident females
choose among visiting extrapair males than that they leave their own territory
to engage in EPCs, although in one study during the egg-laying period females
spent, on average, about 35% of their time more than 100 m from the nest
(Kilpimaa et al., 1995). Such
visits away from the nest may mainly be motivated by foraging but may also
provide opportunities for EPCs.
We may ask if the quality differences between initial and final mates were large enough to be important. In general, final males arrived later than initial mates. However, in many cases the plumage color and/or song complexity of final mates was similar or better than that of initial mates. This may have been caused by better mating options available and/or from increased knowledge of the males in the area and improved ability to assess male quality. High quality of final males may explain why some females did not engage in EPCs. However, the incomplete knowledge hypothesis cannot explain why little EPP was found in cases where females ended up with low-quality males. The point should be further addressed when more is known about the possible benefits females gain from EPCs in this species.
Because initial mates had their own social mate and nest, they may have
been too busy to engage in EPCs. However, this explanation can be rejected
because our manipulation resulted in many instances where females of initial
mates had already passed the period when focal females were fertile
(Figure 1). The period of peak
female fertility seems to be short in pied flycatchers, only lasting from
about 2 days before the first egg is laid until the day the first egg is laid
(Birkhead et al., 1997;
Lifjeld et al., 1997).
It has been suggested that males may reduce their parental effort in
response to cuckoldry (Møller,
1988; Westneat and Sherman,
1993). A previous study of the present population of pied
flycatchers, in which mate switching was experimentally induced in the
female's fertile period by male removals, supported this idea
(Lifjeld et al., 1998).
However, such a risk would hardly prevent females from engaging in EPCs under
natural conditions because intensity of male mate-guarding is low in the
present population (Chek et al.,
1996), making it difficult for males to know that their mate has
copulated with another male.
Finally, benefits supposed to be gained from EPC may be less important in
pied flycatchers than in some other bird species. These benefits may include
increased genetic quality of the offspring (e.g.,
Brown, 1997;
Johnsen et al., 2000). We
found that broods with EPY produced no more recruits to the subsequent
breeding population than broods without EPY. A stronger test would be to
compare recruitment of chicks from the same brood. There were too few broods
available for such an analysis, but local recruitment was no higher for EPY
than for their half-sibs in two species of tits (Parus major, P.
caeruleus; Kempenaers et al.,
1997; Krokene et al.,
1998; Lubjuhn et al.,
1999). In the collared flycatcher Ficedula albicollis,
fledging condition was higher for EPY than for their half-sibs, but local
recruitment was not studied (Sheldon et
al., 1997).
In two of the four experimental cases with EPP, the initial mate was
identified to be the cuckolder. This was more than expected if the four
females copulated with a randomly chosen male in the vicinity. We can probably
reject the idea that these females had stored sperm from the mating period
with the initial mate because of the long time interval from our removal of
the focal female to her final egg laying (7 and 14 days; cf.
Birkhead et al., 1997).
We conclude that our manipulation of female settlement did not result in increased levels of EPP, but when EPP did occur the cuckolder tended to be a familiar male (the initial mate). We recommend that the latter finding be further tested in species where the frequency of EPP is higher than in pied flycatchers.
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ACKNOWLEDGEMENTS |
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We are indebted to the late H. Rinden for assistance in the field and also to W. Johansen, R. Fjeld Karlsen, and C. Listøen Lerberg.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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