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Behavioral Ecology Vol. 11 No. 4: 378–386
Nest and mate choice in the red bishop
(Euplectes orix): female settlement rules
Thomas W. P. Friedl and Georg M. Klump
Institut für Zoologie, Technische Universität München, Lichtenbergstr. 4, D-85747 Garching, Germany
We investigated female settlement in a colony of red bishops (Euplectes orix), a territorial and highly polygynous weaverbird
widely distributed over sub-Saharan Africa. An earlier study showed that male reproductive success is mainly determined by the
number of nests a male builds in his territory, which appeared to be a good indicator of male quality. Because males provide
no parental care or food resources within the territory, females sharing a territory do not compete for material resources and
might therefore be expected to settle preferentially in territories of males that build many nests to gain the possible genetic
benefit of high-quality offspring. An analysis of female settlement, however, revealed that females did not show a preference for
territories of males with many nests and that the distribution of female breeding attempts with regard to the number of vacant
nests within a territory could be explained best by random female settlement in 3 out of 4 years. Females settled more often
than expected by chance (in 3 out of 4 years) in territories already containing occupied nests, indicating that resident females
did not discourage settlement of additional females. However, sharing a territory with other females might impose costs in terms
of an increased predation risk because nests in territories that contained other nests with young suffered from higher predation
than nests in territories that did not contain other nests with young. Females therefore might trade the possible benefits of
settling in territories of males with many nests against the costs of sharing a territory with other females. This might result in
the mating pattern found with random female settlement and male reproductive success being directly proportional to the
number of nests built. We discuss possible implications of this mating pattern for sexual selection on males. Key words: Euplectes
orix, female choice, male quality, predation, random female settlement, sexual selection, weaverbirds. [Behav Ecol 11:378–386
(2000)]
I
n polygynous species with resource defense polygyny, territorial males provide resources that are important for reproduction such as food or nest sites within the territory to
attract more than one female. Females often have to make a
choice between a male without mate and an already mated
male. If there is variation in the amount or quality of the
resources provided by the males, it might pay for the female
to choose an already mated male with, for example, a better
territory, instead of an unmated male, because the advantage
of higher territory quality outweighs the disadvantage of sharing the territory and the available food within the territory
with another female. If the quality differences among territories are large, this will lead to high variation in male mating
success (polygyny threshold model; Verner and Willson, 1966;
Orians, 1969), and female mating preferences can be explained by direct benefits (e.g., better offspring survival resulting from higher food resources within the territory). In
contrast, in polygynous species, where males provide females
with little material resources, such direct benefits of female
mate choice are less likely to fully explain female mating preferences. Instead, indirect mechanisms as proposed by ‘‘good
genes’’ models of sexual selection may play a more important
role.
We studied sexual selection in the red bishop (Euplectes
orix), a sexually dimorphic and polygynous weaverbird from
Southern Africa. Males in breeding plumage establish and defend territories in reedbeds or bullrush stands around water,
where they construct several nests during a breeding season
to which they try to attract females. Most territories contain
one or more empty nests at any time during the breeding
Address correspondence to T. W. P. Friedl. E-mail: Thomas.
[email protected].
Received 7 April 1999; revised 24 August 1999; accepted 30 October
1999.
2000 International Society for Behavioral Ecology
season. Besides the nests, the males provide no other material
resources such as parental care or food within the territories,
and territory quality appears to be similar between males (at
least in the colony that we studied). Therefore, possible direct
benefits of female mate choice seem to be low, and quality
differences between males should become more important in
forming the females’ mating decisions. More details of red
bishop breeding behavior are given in Craig (1974, 1980) and
Friedl (1998).
The only factor found to be related to male mating success
in the red bishop is the number of nests a male builds on his
territory. Males that built many nests had more nests accepted
by females and sired more offspring than males that built fewer nests (Friedl and Klump, 1999). The number of nests built
by the males is a good indicator of male quality because males
that survived and established a territory in the following season (and thereby demonstrated high quality) built more nests
than males that did not establish a territory in the following
season (Friedl and Klump, 1999). Females do not compete
with each other for nests, paternal care, or food resources
within the territory, and, consequently, the costs for females
of sharing a territory with other females seem to be limited.
By mating preferentially with males that build many nests, female red bishops could gain indirect genetic benefits in terms
of high-quality offspring without incurring high costs from
sharing the territory (given that there is some heritable component of male quality). However, the linear relationship
found between the number of nests built by red bishop males
and the number of nests accepted by females (Friedl and
Klump, 1999) indicates that males that build many nests do
not have a disproportionally high mating success (i.e., that
females do not settle preferentially in territories of males with
many nests). Instead, the linear relationship between the
number of nests built and male mating success might be the
result of either random female settlement or females settling
according to an ideal free distribution (Fretwell and Lucas,
1970). Although the outcome in both cases would be the same
Friedl and Klump • Female settlement in red bishops
(i.e., a linear correlation between the number of nests and
the number of mates), the mechanisms resulting in such an
outcome would be fundamentally different. In the case of random female settlement, females exert no choice at all, while
in the case of female settlement according to an ideal free
distribution, females actively choose the males with the highest available number of empty nests at the time of choice.
In this study we investigated the female perspective of nest
and mate choice in the red bishop in more detail. We analyzed the temporal pattern of female choice of nesting sites
in relation to the number of vacant nests within a territory to
distinguish between random female settlement and female
settlement according to an ideal free distribution. Because the
apparent lack of a female preference for males with many
nests might reflect a trade-off between potential costs and
benefits of mating with males of high quality, we attempted to
identify possible constraints on female choice of nesting sites.
We investigated female choice of nesting sites in relation to
the number of occupied nests within a territory to find out
whether resident females affect further settlement. Furthermore, we analyzed clutch and brood losses in relation to the
number of occupied nests within a territory to find out whether there were costs of sharing a territory with other females
in terms of a higher predation rate. Such costs should influence the female’s decision of where to start a breeding attempt and might explain why female red bishops do not show
a preference for males with many nests.
MATERIALS AND METHODS
Study colony
We studied female breeding behavior and female choice of
nesting sites in a colony of red bishops in the Addo Elephant
National Park, Eastern Cape, South Africa (33⬚26⬘ S, 25⬚45⬘
E) during four consecutive breeding seasons (1993–94 to
1996–97), lasting from October to April. The breeding site
was a small dam (approximately 250 m2) surrounded by bullrushes (Typha capensis) and common reeds (Phragmites australis).
General field methods
Throughout the study, we counted nests daily to search for
new nests built by territorial males; these nests were then
marked with numbered yellow plastic tags that were attached
to reeds or bullrush stems close to the nest. We checked all
tagged nests daily to record laying dates of the eggs, clutch
size, hatching dates, number of hatchlings, and number of
fledglings. Throughout the breeding seasons, detailed observations of territorial behavior and aggressive interactions between males were made to obtain information on the location
of the territories and identities of the territory holders. Based
on these data, we drew territory maps and updated them every other week. Social parents of nestlings were assigned
through behavioral observations, identifying both the owner
of the territory in which the nest was situated and the female
incubating or feeding the brood. Field methods are described
in more detail in Friedl and Klump (1999).
Data analysis
Female settlement in relation to the number of vacant nests
within a territory
We investigated the patterns of female settlement in relation
to the number of vacant nests within a territory by comparing
the actual choice of females with the alternatives available at
the time of choice (Garson, 1980). We considered the laying
379
date of the first egg as the day the choice was made. All breeding attempts for which we did not know the exact laying date
of the first egg were excluded from the analysis (for example,
in the first season we could only commence data collection
about 3 weeks after the breeding season had begun; therefore,
we excluded all breeding attempts that were started in the
first 3 weeks of this season). Because the status of all nests
within the colony on every day during the breeding season
was known (with the exception of the first 3 weeks of the
breeding season 1993–94, see above), we could calculate how
many vacant nests were available within each territory for every day a female made a choice. Nests that were empty on a
day a female laid her first egg but had contained eggs before
were regarded as vacant because in several cases females accepted such nests. In contrast, empty nests that had contained
nestlings before were not regarded as vacant because females
were never observed starting breeding attempts in nests that
had previously contained young (Friedl, 1998).
For every day a female laid her first egg, territories were
assigned to categories according to the number of vacant nests
(i.e., all territories with one vacant nest formed the first category, all territories with two vacant nests formed the second
category, and so on). We calculated the expected probability
of being chosen for every territory category, assuming that
females were occupying nests at random and that the probability of a territory being chosen by a female was proportional
to the number of vacant nests within this territory. A territory
with, for example, two vacant nests had twice the probability
of being chosen compared to a territory with only one vacant
nest, and so on. Thus, the analysis was conducted at the level
of the nests even if we formed and analyzed territory categories. The expected number of females choosing a territory
of a particular category was calculated by dividing the number
of vacant nests available within the territory category by the
total number of nests available on that day and then multiplying the resulting value by the number of breeding attempts
that were started on that day. Summing up the calculated
probabilities for each territory category for every day within
a breeding season on which breeding attempts were started
resulted in the expected total number of nests accepted in
the different territory categories for the entire breeding season. We then compared this expected distribution with the
observed distribution of the number of nests accepted using
chi-square statistics.
Female settlement in relation to the number of occupied nests
within a territory
We analyzed female settlement in relation to the number of
occupied nests within a territory to evaluate effects of resident
females on further female settlement within the same territory. We adopted a similar approach as in the analysis of female settlement in relation to the number of vacant nests described above. All nests that contained eggs or nestlings were
classified as occupied. For every day a female started a breeding attempt, we first combined all territories with the same
number of occupied nests at that particular day to form one
territory category (that is, all territories with no occupied
nests formed the first category, all territories with one occupied nest formed the second category, all territories with two
occupied nests formed the third category, and so on). Territories with no vacant nests on a particular day were excluded
from the analysis for this day. We then calculated the probability for every territory category to be chosen under the assumption of random female settlement with respect to the
number of occupied nests within a territory. That is, we assumed that the probability of a territory category to be chosen
by a female was proportional to the number of available vacant nests within this territory category. The sum over all days
380
in a breeding season on which breeding attempts were started
yielded the expected frequency of nests accepted for the different territory categories. This frequency distribution could
then be compared with the observed distribution of accepted
nests in the different territory categories.
Nest predation in relation to the number of occupied nests
within a territory
To test whether there are costs or benefits of sharing a territory with other females in terms of higher or lower predation
rates, we analyzed predation in relation to the number of occupied nests within a territory. We considered every nest in
which eggs or nestlings were missing compared to the previous day as predated, even if there were no signs of nest damage or destruction. The predominant predator in the study
colony was the cape cobra (Naja nivea), accounting for an
estimated 80–90% of all losses. Cape cobras were often observed moving through the colony and robbing nests, and
nests that were predated by cape cobras never showed any sign
of nest damage (Friedl and Klump, personal observation).
Sometimes predated nests were found with holes in the bottom part of the nest, which is typical for predation by house
rats, Rattus rattus (Craig, 1982). Other potential nest predators common at the study site were boomslang (Dispholidus
typus), grey heron (Ardea cinerea), fiscal shrike (Lanius collaris), small grey mongoose (Galerella pulverulenta) and yellow mongoose (Cynictis penicillata). We calculated a random
predation distribution similar to the random distributions described above. For every day we found nests that were predated, we formed territory categories according to the number of occupied nests within a territory. Territories with no
occupied nests on a particular day were excluded from the
analysis for that day. We then calculated the probability for
every territory category to be affected by predation under the
assumption that predation occurred randomly—that is, that
every occupied nest had the same probability of being predated irrespective of whether there were other occupied nests
within the same territory. We summed up the probabilities for
all days in a breeding season on which nest predation took
place and compared the resulting random predation distribution with the observed frequency distribution of predation
events.
Statistics
All data analyses were conducted using the software package
SPSS/PC (SPSS Inc.). Descriptive statistics are given as means
⫾ standard deviation unless otherwise stated. All p values given are two tailed.
RESULTS
Breeding activity and multiple breeding attempts
During the 4 study years, 1254 nests were recorded. Females
started 670 breeding attempts and laid 1992 eggs; mean clutch
size was 2.973 ⫾ 0.598 (range 1–5 eggs per clutch). A total of
1072 eggs hatched, and 518 nestlings fledged successfully. Out
of 386 individually marked females, 117 were observed starting breeding attempts in the colony. Several females started
more than one breeding attempt within a single breeding season. Because the attending female could not always be identified for breeding attempts that failed early in the breeding
cycle, the observed numbers of females starting multiple
breeding attempts must be regarded as minimum numbers.
Twenty-three of the 117 females (19.7%) started two breeding
attempts within one season, and in 7 cases both attempts were
successful in producing fledglings. In six instances females
started with a second clutch only about 1 week after chicks
Behavioral Ecology Vol. 11 No. 4
from the first brood had left the nest. These females were still
observed feeding the fledglings while at the same time incubating their second clutch. Seven females produced a replacement clutch soon after the eggs from their first clutches disappeared. This can be as soon as 10 days after the start of the
first clutch (median 16 days, range 10–22 days). These females
never used the same nest for the replacement clutch. In fact,
in five out of the seven cases the replacement clutch was laid
in a different territory. Two females (1.7%) started three
breeding attempts within a season. Both of them first produced hatchlings that were predated, while in the second and
third breeding attempt the eggs disappeared before the
hatching date. The time spans between the start of the first
and second breeding attempt were 23 and 46 days, and between the second and third attempt 20 and 19 days. One female (0.9%) even started four breeding attempts within a single season, with the first two producing fledglings; in the last
two the eggs disappeared before hatching. Time spans between the four breeding attempts were 34 days, 44 days, and
11 days, respectively.
Female settlement in relation to the number of vacant nests
To be able to distinguish between random female settlement
and female nest choice according to an ideal free distribution,
we compared the observed distribution of breeding attempts
among territories with a different number of vacant nests with
the expected distribution of breeding attempts calculated under the assumption of random female settlement (i.e., under
the assumption that every vacant nest had the same probability of being chosen; see Methods). Female nest choice according to an ideal free distribution predicts that females choose
the territories with the highest number of available vacant
nests at the time they make their choice. That is, for the territory categories with many vacant nests, the observed frequency of breeding attempts should be higher than the expected frequency calculated under the assumption of random
female settlement. The results from the analysis of 521 breeding attempts in the four study seasons, presented in Table 1,
clearly show that this is not the case. Territory categories with
many vacant nests were mostly chosen less often than expected by chance, indicating that the pattern of female settlement
cannot be explained by female choice of nesting sites according to an ideal free distribution. In three out of the four seasons investigated, the observed distribution of breeding attempts was not significantly different from the distribution expected by chance, suggesting that in these three seasons the
observed pattern of breeding attempts can be explained by
random female settlement. Only in the breeding season 1996–
97 was the observed distribution of breeding attempts significantly different from the distribution calculated under the
assumption of equal probabilities of being chosen for all vacant nests within the colony (see Table 1).
Female settlement in relation to the number of occupied
nests
To see whether the females’ mating decisions were affected
by the number of other females breeding within the territories, we compared the observed distribution of breeding attempts with the distribution calculated under the assumption
that every nest has the same probability of being chosen independently of the number of occupied nests within a territory at the time of choice (see Methods). If females started
breeding attempts in territories with many occupied nests
more often than expected by chance, this would indicate that
females actively chose such territories. If, on the other hand,
females were observed to breed less often in territories with
Friedl and Klump • Female settlement in red bishops
381
Table 1
Observed distribution of breeding attempts compared with the distribution expected under the assumption of random female settlement
with regard to the number of vacant nests within a territory
Season
Number of vacant nests within a territory
1
2
3
4
1993–94
Expected
Observed
30.16
35
24.3
22
17.05
13
1994–95
Expected
Observed
36.72
43
68.8
72
49.23
46
1995–96
Expected
Observed
13.69
17
29.48
28
1996–97
Expected
Observed
34.39
28
42.63
70
3.34
5
5
6
7
␹2
Total
p
0.15
0
75
2.776
.428
23.0
17
5.25
5
183
3.013
.556
21.74
19
16.46
16
4.63
6
86
1.638
.802
39.32
45
32.06
24
177
35.189
.0005
17.4
8
occupied nests than expected by chance, this would present
evidence for females actively avoiding territories with already
breeding females. The analysis revealed that in the breeding
season 1995–96 the observed distribution was almost equal to
the distribution expected by chance, indicating that in this
season females settled at random with respect to the number
of occupied nests within a territory (Table 2). In the three
breeding seasons 1993–94, 1994–95, and 1996–97, the observed distribution of breeding attempts was significantly different from the distribution expected by chance (Table 2). In
all three seasons this difference seemed to be caused by territories with no occupied nests being chosen less often than
expected by chance. To test this, we performed a second analysis with only two territory categories (i.e., territories with and
without occupied nests). The results confirmed that in the
breeding seasons 1993–94 and 1996–97 territories without occupied nests were chosen significantly less often than expected by chance (breeding season 1993/94: ␹2 ⫽ 21.98, p ⬍ .001;
breeding season 1996–97: ␹2 ⫽ 5.21, p ⫽ .022). The same
tendency was found in the season 1994–95; however, observed
and expected distribution were not significantly different
from each other in this season (␹2 ⫽ 1.125, p ⫽ .289).
10.37
1
0.83
1
Predation in relation to the number of occupied nests
If the predation rate is influenced by the number of breeding
females within a territory, females should either actively seek
territories with already breeding females or avoid such territories, depending on whether the number of simultaneously
breeding females decreases or increases the predation risk.
We tested for effects of the number of simultaneously breeding females on predation rate by comparing the observed distribution of predation events with the frequency distribution
calculated under the assumption that every occupied nest has
the same probability of being predated (see Methods). There
was no significant difference between the observed distribution and the calculated random distribution of predation for
any of the four breeding seasons (Table 3), suggesting that
predation risk was not related to the number of occupied
nests within a territory. However, since predators might be
more easily attracted by nestlings than by eggs, we performed
a second analysis considering only nests that contained young.
For this analysis territories were classified in only two categories (i.e., territories with and without nests containing nestlings). We then tested whether the observed probability of an
Table 2
Observed distribution of breeding attempts compared with the distribution expected under the assumption of random female settlement
with regard to the number of occupied nests within a territory
Number of occupied nests within a territory
Season
0
1
2
3
1993–94
Expected
Observed
39.28
19
15.35
28
14.47
21
1994–95
Expected
Observed
55.59
49
48.44
48
42.93
39
1995–96
Expected
Observed
51.15
50
26.17
24
6.75
9
1.68
3
0.25
0
1996–97
Expected
Observed
57.23
43
48.47
41
29.99
48
24.83
28
10.21
9
4.73
6
22.2
24
4
5
6
0.1
1
0.53
0
0.54
0
9.63
14
2.23
6
1.76
2
2.93
2
2.53
3
7
0.15
1
0.55
3
8
0.07
0
0.26
0
␹2
p
75
31.807
.0005
183
14.491
.043
86
1.986
.575
177
27.295
.0005
Total
Behavioral Ecology Vol. 11 No. 4
382
Table 3
Observed distribution of nest-predation events compared with the distribution expected under the assumption of random nest predation with
regard to the number of occupied nests within a territory
Number of occupied nests within a territory
Season
1
2
3
4
5
6
1993–94
Expected
Observed
21.82
22
40.72
35
29.99
27
9.55
12
5.0
11
0.91
1
1994–95
Expected
Observed
23.3
23
34.7
42
22.56
22
14.25
11
1995–96
Expected
Observed
37.38
45
23.45
19
11.45
10
5.72
4
1996–97
Expected
Observed
26.23
23
28.56
42
31.54
26
14.95
10
4.32
4
4.49
6
occupied nest (both nests with eggs and/or young) being predated was affected by the presence or absence of nests containing young within a territory. The results of this second
analysis are shown in Table 4. In three out of the four seasons
nests in territories with nestlings suffered higher predation
rates than expected by chance. In the season 1993–94 the
difference from a random distribution was statistically significant, whereas in the seasons 1994–95 and 1996–97, despite a
similar trend, there was no significant difference from the calculated random distribution. Only in the season 1995–96 were
observed predation rates similar to the predation rates expected by chance. These data suggest that at least in some
years sharing a territory with other females might impose costs
in terms of an increased predation risk.
DISCUSSION
Polygyny and female nest and mate choice in birds
In polygynous mating systems with female choice of mates and
nesting sites, female settlement rules should depend on the
Table 4
Observed distribution of nest-predation events compared with the
distribution expected under the assumption of random nest
predation with regard to whether there were nests with young within
a territory
Season
Territories
without
nestlings
Territories
with
nestlings Total
␹2
p
1993–94
Expected
Observed
61.13
35
46.87
73
108
25.737
.0005
1994–95
Expected
Observed
46.23
38
57.77
66
104
2.638
.104
1995–96
Expected
Observed
51.72
51
26.28
27
78
0.03
.863
1996–97
Expected
Observed
42.16
34
68.84
77
111
2.547
.111
3.56
2
4.05
2
7
8
1.27
0
0.46
1
0.77
1
Total
␹2
p
108
8.94
.111
104
2.955
.707
78
3.099
.377
111
11.616
.114
amount of material or genetic benefits provided by the males.
In resource-defense polygyny, males often provide paternal
care and/or food resources within the territory. The degree
of polygyny in such a species will then be determined by the
relative importance of these unshareable material benefits for
female reproductive success. If male parental care is essential
for successfully rearing young, the degree of polygyny should
be low because females settling in the same territory compete
for paternal care. Such competition can lead to a lower reproductive success of secondary females compared to monogamous or primary females due to reduced male assistance in
feeding nestlings or nest defense, as has been demonstrated
for several species (e.g., Alatalo and Lundberg, 1990; Catchpole et al., 1985; Johnson et al., 1993; Kempenaers, 1994;
Smith et al., 1994; Veiga, 1990). If, on the other hand, male
assistance in feeding young is limited and not essential for
nestling survival, the costs for females sharing a territory with
other females are low, and a higher degree of polygyny is to
be expected. This expectation was confirmed by Searcy and
Yasukawa (1995), who presented data on male contribution
to feeding of nestlings and the degree of polygyny for 10 populations of 8 polygynous passerines. They found a negative
correlation between these two variables; that is, as male contribution to feeding the nestlings decreases, the degree of polygyny increases.
The relative importance of unshareable material benefits
provided by males for female reproductive success should not
only affect the degree of polygyny but also female matesearching behavior. In species in which females suffer high
costs of being secondary females of polygynous males, they
should sample males to gather information on their mating
status to avoid mating with an already mated male. In species
in which females suffer low costs of sharing a male’s territory
with other females, they should reduce or even cease matesampling behavior; that is, they should settle randomly with
respect to the available nesting sites. Lightbody and Weatherhead (1987b, 1988) proposed a ‘‘neutral mate-choice’’ model to explain polygynous mating in species where females neither suffer nor gain from sharing territories with other females. This model assumes that females settle independently
of each other and independently of variation in male or territory quality. In support of this hypothesis, Lightbody and
Weatherhead (1987a,b) presented data from a population of
highly polygynous, marsh-nesting yellow-headed blackbirds
(Xanthocephalus xanthocephalus), suggesting that (1)paternal
Friedl and Klump • Female settlement in red bishops
care is limited and not essential for nestling survival, and (2)
females settled independently from each other and did not
affect each other’s reproductive success. Similarily, Hartley
and Shepherd (1995) presented evidence for random female
settlement in the corn bunting (Miliaria calandra), in which
polygyny is apparently not costly to females (Hartley and
Shepherd, 1994).
Is there evidence for nonrandom nest choice?
Since in the red bishop males provide no parental care or
food resources within the territories, and since the territories
appear to be of rather uniform quality, both a high degree of
polygyny and restricted or even absent female mate-searching
behavior is to be expected (see above). In a study on determinants of male reproductive success in the red bishop, we
could indeed show that the degree of polygyny is extremely
high in this species, with some males mating with up to 18
females within a single breeding season (Friedl and Klump,
1999). Furthermore, we found a linear relationship between
the number of nests built by the males and their reproductive
success, indicating that females might settle randomly with
respect to available nests within the breeding colony (Friedl
and Klump, 1999). The detailed analysis of female settlement
in relation to the number of vacant nests within a territory
confirmed that females in three out of four seasons settled
randomly with respect to the number of available nests within
territories (see Table 1). The alternative possibility, that the
linear relationship between the number of nests built by the
males and their reproductive success is the result of females
choosing territories according to an ideal free distribution
(see Introduction), was not supported by our data (Table 1).
We have no explanation for the strong departure of female
settlement from random with regard to nest availability in the
season 1996–97; there was no obvious difference between this
season and the other three seasons (for example, the breeding season 1994–95 was characterized by a similar high breeding activity in terms of the number of breeding attempts; see
Table 1).
Evans and Burn (1996) analyzed female settlement rules in
the wren (Troglodytes troglodytes), a small monomorphic passerine with high levels of polygyny. The mating system of the
wren is similar to that of the red bishop; male wrens defend
small territories where they build several nests to which they
try to attract females, and male mating success has been found
to be correlated with the number of nests built by the males
(Evans and Burn, 1996). Using a similar type of analysis as we
did in this study, Evans and Burn (1996) found that territories
with many vacant nests were chosen significantly more frequently than expected by chance, and they concluded that
females were more likely to nest on territories with large numbers of vacant nests. Furthermore, they showed that the probability of a nest being occupied by a female was independent
of the number of other vacant nests on the territory (i.e.,
every nest had the same probability of attracting a female).
As pointed out by Evans and Burn (1996), these findings
could be interpreted as the result of females using a random
settlement rule, similar to what we found in the red bishop.
Random female mating and sexual selection
As we have shown, female red bishops mostly settle randomly
with respect to the number of vacant nests within the territories. What are the effects of such settlement rules on the
males? It is clear that under random female settlement, males
that build many nests obtain a higher mating success simply
by chance. Even without any female preferences, there will be
a strong sexual selection on males to build as many nests as
383
possible. The number of nests built will then be limited by
energetic and time constraints, which per se will act differently on males, depending on male quality and condition.
The number of nests built by red bishop males has been
shown to be a good indicator of male quality; males that survived and established a territory in the following season built
more nests than males that did not establish a territory in the
following season (Friedl and Klump, 1999). Janetos (1980)
presented a theoretical analysis of different female matechoice strategies and found random mating to be the worst
strategy, with the average fitness or quality of males chosen
being equal only to the mean of the male population, while
other mate-choice strategies like ‘‘fixed-threshold decisions’’
and ‘‘best-of-n-males’’ consistently resulted in an average quality of males chosen above the mean of the population. However, the model assumed a mating system in which random
mating results in an equal probability of every male being
chosen irrespectively of male quality. This is in contrast to the
mating pattern found in the red bishop, where random mating results in high-quality males having a higher probability
of being chosen because they offer more nests than low-quality males. Thus, in the red bishop the average expected fitness
of males chosen by females adopting a random settlement
rule is above the mean of the male population, and females
therefore have a good chance of getting a high-quality mate
without incurring any costs of mate-searching behavior.
Even without female choice there can be strong sexual selection on males. In fact, such a pattern might be common
and could explain highly biased male reproductive success in
many species in which males provide little or no material resources and for which there is no evidence of active female
mate choice (see also Sutherland, 1985). In many bird species
it has been shown that male territory size is an important
factor determining male reproductive success (for review, see
Andersson, 1994). Random female settlement would result in
males with larger territories getting more mates and, consequently, there would be strong sexual selection for males to
establish and defend breeding territories as large as possible.
Because males that are able to defend large territories are
probably males of good condition and/or high quality, females would have a good chance of mating with high-quality
males even if they settled randomly (Lightbody and Weatherhead, 1988). Random female mate acquisition might also
best explain the mating system found in many lek-breeding
birds, anurans, and insects, in which lek attendance has been
shown to be the most important factor determining male mating success (for review, see Andersson, 1994; Höglund and
Alatalo, 1995). In lekking species males provide no material
benefits but only their genes to the next generation (Höglund
and Alatalo, 1995), and intrasexual selection often takes the
form of endurance rivalry (see Andersson, 1994). A random
female mating pattern would result in a considerable skew in
male mating success, with males with the highest lek attendance obtaining most matings, an outcome that is typical for
many lek-breeding species (Höglund and Alatalo, 1995). Random female mating in leks would select for males that stay at
the lek as long as possible, with males of better condition and
higher quality being able to attend the lek for longer than
others.
Random females settlement is, however, not restricted to
species in which males provide little or no material resources
to the females they mate with. For example, Dale and Slagsvold (1990) presented evidence for random female settlement
in the pied flycatcher (Ficedula hypoleuca), a polygynous passerine in which female reproductive success depends heavily
on male help in nestling provisioning (e.g., Alatalo and Lundberg, 1990), and secondary females receive less male assistance than primary females (Alatalo et al., 1982). Thus, ran-
384
dom female settlement in the pied flycatcher cannot be explained by the neutral mate-choice model proposed by Lightbody and Weatherhead (1987b, 1988), which assumes no costs
of mating with an already mated male (see above). Instead,
Dale and Slagsvold (1990) suggested that random female settlement in this species might best be explained by high costs
of searching for a better mate.
Do resident females affect further settlement?
Our results demonstrated that female red bishops mostly (in
three out of four seasons) settle randomly with respect to the
number of vacant nests within the territory, despite the fact
that they could get high-quality males if they would actively
choose males with many nests. So why don’t they show a clear
mating preference for males with many nests? One possible
explanation could be that female settlement is restricted by
female–female aggression. In polygynous species in which female reproductive success relies on male parental effort, there
are conflicting interests of primary and secondary females because they compete for male assistance in nestling provisioning. Resident females should try to discourage or at least delay
further settlement to obtain as much male help as possible
for their own brood. Delayed settlement of secondary females
has been shown to be advantageous for primary females because males of several polygynous species direct more of their
parental care toward the second brood if the hatching interval
between first and second brood is short (Bruun et al., 1997;
Kempenaers, 1995; Lifjeld and Slagsvold, 1990; Sandell et al.,
1996; Smith et al., 1994; but see Leonard, 1990). Indeed, aggressive behavior of resident females toward female intruders
has been reported for numerous species (see review by Slagsvold and Lifjeld, 1994). There are other possible benefits that
might select for female–female aggressiveness even in polygynous species like the red bishop, in which there is no competition among females for male parental care or food resources within the territory. For example, by discouraging other females from breeding in the same territory, nests would
be spaced out more, which might reduce predation risk. Furthermore, female–female aggression might prevent intraspecific nest parasitism. On the other hand, polygyny might be
beneficial to females. One possible benefit could be increased
safety from nest predation due to either joint nest defense or
dilution of predatorial attempts. Joint nest defense of females
sharing a breeding territory against conspecific female intruders might also decrease the risk of intraspecific nest parasitism.
Our analysis of female settlement in relation to the number
of occupied nests within a territory in the red bishop showed
that in one out of four seasons female settlement was random
with respect to the number of resident females, whereas in
the other three seasons territories without occupied nests
were chosen less often than expected by chance (Table 2).
The finding that females were more likely to nest on territories already containing another nesting female could have
been the result of females avoiding territories of inferior quality. However, because all the territories in the breeding colony
were rather uniformly structured patches of reedbeds and
bullrush stands, and therefore territory quality appeared to
be similar between males, this explanation seems unlikely. In
any case, our data demonstrate that there is no negative effect
of resident females on further settlement because females settled not less often than expected by chance in territories with
many resident females. Thus, the fact that female red bishops
did not choose males that built many nests more often than
expected by chance cannot be explained by a discouraging
effect of resident females on further settlement.
Behavioral Ecology Vol. 11 No. 4
Is the predation risk influenced by the number of breeding
females within a territory?
Another possible reason for the absence of a clear female mating preference for males with many nests could be that sharing a territory with other females, and thereby increasing nest
density, might increase predation risk. Indeed, in our study
colony the probability of a nest being predated was significantly higher for nests in territories that contained other nests
with nestlings than for nests in territories that did not contain
other nests with nestlings in one season, and in two more
seasons there was a nonsignificant tendency in the same direction (Table 4). Only in the season 1995–96 did nest predation events appear to be random with respect to whether
or not there were other nests with nestlings within the territory. The season 1995–96 was also the only season in which
we found random female settlement with regard to the number of occupied nests within a territory (see Table 2). We
think that this might be due to the fact that overall breeding
activity was much lower in 1995–96 than in the other three
seasons, with only 86 breeding attempts in 1995–96 compared
to more than 150 breeding attempts in the other seasons.
Our findings of an increased predation risk for nests in
territories that contain other nests with nestlings are in contrast to those reported by Picman et al. (1988) on effects of
nest clumping on predation risk in marsh-nesting red-winged
blackbirds. They placed groups of artificial nests with eggs
either near (experimental groups) or away (control groups)
from an active redwing nest and found that the experimental
groups of nests suffered less predation compared to the control groups. Similarily, Westneat (1992) found in another population of red-winged blackbirds that increased breeding synchrony lowered the probability of nest predation. We think
that the different effects of nest density on predation risk
found in our study on red bishops compared to the studies
on red-winged blackbirds by Picman et al. (1988) and Westneat (1992) are probably due to different types of predators.
The main predators in the red-winged blackbird colony studied by Picman et al. (1988) were marsh wrens (Cistothorus
palustris), which could be displaced through aggressive behavior by redwings (Picman et al., 1988). Predation by marsh
wrens in this population should decrease with increasing nest
density simply because the probability of detecting the marsh
wrens is higher if more females are nesting within the same
territory. At the breeding site of the redwing population studied by Westneat (1992), both mammalian predators (raccoons, Procyon lotor; short-tailed weasels, Mustela erminea;
mink, Mustela vison) and avian predators (American crows,
Corvus brachyrhynchos; blue jays, Cyanocitta cristata; common
grackles, Quiscalus quiscula) were common. Here the decrease of predation risk with increasing breeding synchrony
might be due both to a dilution effect on mammalian predators and to mutual nest defense against avian predators. At
our study colony of red bishops the main predators were cape
cobras. We never observed physical attacks of red bishops
against cape cobras, and even intense mobbing by colony
members did not prevent the cobras from robbing nests. Furthermore, cape cobras are opportunistic feeders and exploit
food sources such as a red bishop breeding colony more with
higher food availability (Friedl and Klump, personal observations). Therefore, predation risk in our study colony is unlikely to be reduced by mutual nest defense or dilution effects,
which might explain why we found—contrary to the studies
on red-winged blackbirds—an increased predation risk of
nests in territories that contained other nests with young.
Conclusions
We have shown that in the red bishop, a colonial polygynous
passerine, female settlement appears to be random (in three
Friedl and Klump • Female settlement in red bishops
out of four seasons) with respect to nest availability, with every
vacant nest in the colony having the same probability of being
chosen. Females showed no clear preference for territories of
males that built many nests, although they might benefit from
such a preference because the number of nests built is a good
indicator of male quality (Friedl and Klump, 1999). The lack
of a clear preference for territories of high-quality males could
not be explained by a discouraging effect of resident females
on further settlement because in three out of four seasons
females settled more often than expected by chance in territories that contained already nesting females. However, it
might be explained by costs of sharing a territory with other
females in terms of an increased predation risk for nests if
there are other nests containing nestlings within the same territory. Females therefore face a trade-off between possible
benefits of breeding in territories of high-quality males in
terms of high-quality offspring (if there are heritable components of male quality) and costs of sharing these territories
with other females in terms of an increased predation risk.
This could lead to the observed mating pattern with apparent
random female settlement and male mating success being directly proportional to the number of nests built within the
territory.
However, female choice of a copulation partner is not necessarily restricted to the social mate (i.e., to the owner of the
territory where the females started their breeding attempts).
In many bird species extrapair copulations are common, and
they often result in high proportions of young sired by males
other than the social mate (Birkhead and Møller, 1992). Females of several species have been reported to control or even
actively seek extrapair copulations (e.g., Gray, 1996; Houtman,
1992; Lifjeld and Robertson, 1992; Neudorf et al., 1997; Sheldon, 1994; Smith, 1988; Venier et al., 1993). Furthermore,
females have been shown to selectively solicit extrapair copulations from males that are of higher quality than their social
mates, consistent with the hypothesis that females solicit extrapair copulations to enhance the genetic quality of their
offspring (Graves et al., 1993; Hasselquist et al., 1996; Houtman, 1992; Kempenaers et al., 1992; Otter et al., 1998; Weatherhead and Boag, 1995). The proportion of extrapair young
in the red bishop colony we studied in Addo was 17.6%, and
30.5% of all broods contained at least one extrapair young,
as determined by multilocus DNA fingerprinting (Friedl,
1998; Friedl and Klump, 1999). Since in red bishops females
control copulations and male mate guarding is absent, the
relatively high proportion of extrapair young highlights the
potential for females to modify their mate choice by selectively
seeking copulations with males other than their social mates.
Thereby they could at least in part escape the limitations set
by the choice of a nesting site and hence a social mate.
We thank Mike Cherry and Horst Klump for support in different
phases of this field project. Adrian Craig and Albert Schultz helped
with mist netting in the field. We are grateful to the National Parks
Board of South Africa for permission to conduct this study in the
Addo Elephant National Park, and the whole park staff for continuous
support. The comments of Matthew R. Evans, Ken Norris, Ulrike Langemann, and an anonymous referee on a previous version of the manuscript are gratefully acknowledged. T.W.P.F. was supported by grants
from the DAAD, the Friedrich-Schiedel-Stiftung, the Stifter-Verband,
and by a scholarship from the Technical University Munich. This
study was supported in part by a grant from the Deutsche Forschungsgemeinschaft (Kl 608/11-1).
REFERENCES
Alatalo RV, Lundberg A, 1990. Polyterritorial polygyny in the pied
flycatcher. Adv Study Behav 19:1–27.
385
Alatalo RV, Lundberg A, Stahlbrandt K, 1982. Why do pied flycatcher
females mate with already mated males? Anim Behav 30:585–593.
Andersson M, 1994. Sexual selection. Princeton, New Jersey: Princeton University Press.
Birkhead TR, Møller AP, 1992. Sperm competition in birds: evolutionary causes and consequences. London: Academic Press.
Bruun M, Sandell MI, Smith HG, 1997. Polygynous male starlings
allocate parental effort according to relative hatching date. Anim
Behav 54:73–79.
Catchpole CK, Leisler B, Winkler H, 1985. Polygyny in the great reed
warbler, Acrocephalus arundinaceus: a possible case of deception.
Behav Ecol Sociobiol 16:285–291.
Craig AJFK, 1974. Reproductive behaviour of the male red bishop
bird. Ostrich 45:149–160.
Craig AJFK, 1980. Behaviour and evolution in the genus Euplectes. J
Ornithol 121:144–161.
Craig AJFK, 1982. Breeding success of a red bishop colony. Ostrich
53:182–188.
Dale S, Slagsvold T, 1990. Random settlement of female pied flycatchers, Ficedula hypoleuca: significance of male territory size. Anim Behav 39:231–243.
Evans MR, Burn JL, 1996. An experimental analysis of mate choice in
the wren: a monomorphic, polygynous passerine. Behav Ecol 7:101–
108.
Fretwell SD, Lucas HL, 1970. On territorial behaviour and other factors influencing habitat distribution in birds. Acta Biotheor 19:16–
36.
Friedl TWP, 1998. Sexual selection in the red bishop (Euplectes orix)
(doctoral dissertation). München: Technische Universität München.
Friedl TWP, Klump GM, 1999. Determinants of male mating success
in the red bishop (Euplectes orix). Behav Ecol Sociobiol 46:387–399.
Garson PJ, 1980. Male behaviour and female choice: mate selection
in the wren? Anim Behav 28:491–502.
Graves J, Ortega-Ruano J, Slater PJB, 1993. Extra-pair copulations and
paternity in shags: do females choose better males? Proc R Soc
Lond B 253:3–7.
Gray EM, 1996. Female control of offspring paternity in a western
population of red-winged blackbirds (Agelaius phoeniceus). Behav
Ecol Sociobiol 38:267–278.
Hartley IR, Shepherd M, 1994. Female reproductive success, provisioning of nestlings and polygyny in corn buntings. Anim Behav 48:
717–725.
Hartley IR, Shepherd M, 1995. A random female settlement model
can explain polygyny in the corn bunting. Anim Behav 49:1111–
1118.
Hasselquist D, Bensch S, von Schantz T, 1996. Correlation between
male song repertoire, extra-pair paternity and offspring survival in
the great reed warbler. Nature 381:229–232.
Höglund J, Alatalo RV, 1995. Leks. Princeton, New Jersey: Princeton
University Press.
Houtman AM, 1992. Female zebra finches choose extra-pair copulations with genetically attractive males. Proc R Soc Lond B 249:3–6.
Janetos AC, 1980. Strategies of female mate choice: a theoretical analysis. Behav Ecol Sociobiol 7:107–112.
Johnson LS, Kermott LH, Lein MR, 1993. The cost of polygyny in the
house wren Troglodytes aedon. J Anim Ecol 62:669–682.
Kempenaers B, 1994. Polygyny in the blue tit: unbalanced sex ratio
and female aggression restrict mate choice. Anim Behav 47:943–
957.
Kempenaers B, 1995. Polygyny in the blue tit: intra- and inter-sexual
conflicts. Anim Behav 49:1047–1064.
Kempenaers B, Verheyen GR, Van den Broeck M, Burke T, Van
Broeckhoven C, Dhondt AA, 1992. Extra-pair paternity results from
female preferences for high-quality males in the blue tit. Nature
357:494–496.
Leonard ML, 1990. Polygyny in marsh wrens: asynchronous settlement as an alternative to the polygyny-threshold model. Am Nat
136:446–458.
Lifjeld JT, Robertson RJ, 1992. Female control of extra-pair fertilization in tree swallows. Behav Ecol Sociobiol 31:89–96.
Lifjeld JT, Slagsvold T, 1990. Manipulations of male parental investment in polygynous pied flycatchers, Ficedula hypoleuca. Behav Ecol
1:48–54.
Lightbody JP, Weatherhead PJ, 1987a. Interactions among females in
386
polygynous yellow-headed blackbirds. Behav Ecol Sociobiol 21:23–
30.
Lightbody JP, Weatherhead PJ, 1987b. Polygyny in the yellow-headed
blackbird: female choice versus male competition. Anim Behav 35:
1670–1684.
Lightbody JP, Weatherhead PJ, 1988. Female settling patterns and polygyny: tests of a neutral-mate-choice hypothesis. Am Nat 132:20–
33.
Neudorf DL, Stutchbury BJM, Piper WH, 1997. Covert extraterritorial
behavior of female hooded warblers. Behav Ecol 8:595–600.
Orians GH, 1969. On the evolution of mating systems in birds and
mammals. Am Nat 103:589–603.
Otter K, Ratcliffe L, Michaud D, Boag PT, 1998. Do female blackcapped chickadees prefer high-ranking males as extra-pair partners? Behav Ecol Sociobiol 43:25–36.
Picman J, Leonard M, Horn A, 1988. Antipredation role of clumped
nesting by marsh-nesting red-winged blackbirds. Behav Ecol Sociobiol 22:9–15.
Sandell MI, Smith HG, Bruun M, 1996. Paternal care in the European
starling, Sturnus vulgaris: nestling provisioning. Behav Ecol Sociobiol 39:301–309.
Searcy WA, Yasukawa K, 1995. Polygyny and sexual selection in redwinged blackbirds. Princeton, New Jersey: Princeton University
Press.
Behavioral Ecology Vol. 11 No. 4
Sheldon BC, 1994. Sperm competition in the chaffinch: the role of
the female. Anim Behav 47:163–173.
Slagsvold T, Lifjeld JT, 1994. Polygyny in birds: the role of competition
between females for male parental care. Am Nat 143:59–94.
Smith HG, Ottosson U, Sandell M, 1994. Intrasexual competition
among polygynously mated female starlings (Sturnus vulgaris). Behav Ecol 5:57–63.
Smith SM, 1988. Extra-pair copulations in black-capped chickadees:
the role of the female. Behaviour 107:15–23.
Sutherland WJ, 1985. Chance can produce a sex difference in variance in mating success and explain Bateman’s data. Anim Behav
33:1349–1352.
Veiga JP, 1990. Sexual conflict in the house sparrow: interference between polygynously mated females versus asymmetric male investment. Behav Ecol Sociobiol 27:345–350.
Venier LA, Dunn PO, Lifjeld JT, Robertson RJ, 1993. Behavioural patterns of extra-pair copulation in tree swallows. Anim Behav 45:412–
415.
Verner J, Willson MF, 1966. The influence of habitats on mating systems of North American passerine birds. Ecology 47:143–147.
Weatherhead PJ, Boag PT, 1995. Pair and extra-pair mating success
relative to male quality in red-winged blackbirds. Behav Ecol Sociobiol 37:81–91.
Westneat DF, 1992. Nesting synchrony by female red-winged blackbirds: effects on predation and breeding success. Ecology 73:2284–
2294.