Behavioral Ecology Vol. 10 No. 2: 185–190
Brood desertion in Kentish plover: sex
differences in remating opportunities
Tamás Székely,a,b Innes C. Cuthill,a and János Kisc
Centre for Behavioural Biology, School of Biological Sciences, University of Bristol, Woodland Road,
Bristol, BS8 1UG, UK, bBehavioural Ecology Research Group, Department of Zoology, Kossuth
University, Debrecen, H-4010, Hungary, and cDepartment of Ethology, Eötvös University, Jávorka u.
14., H-2131 Göd, Hungary
a
To understand the evolution of parental care, one needs to estimate the payoffs from providing care for the offspring and the
payoffs from terminating care and deserting them. These payoffs are rarely known. In this study we experimentally estimated
the rewards from brood desertion in a species that has a variable pattern of parental care. In particular, either the female or
the male parent may desert the brood in Kentish plover Charadrius alexandrinus, so some broods are attended by one parent
of either sex, whereas in other broods both parents stay with the brood until the chicks fledge. We created single males and
single females by experimentally removing the other parent and the clutch. The expected remating time of males was significantly higher (median: 25.4 days) than that of the females (5.3 days, p , .0001). The expected remating time tended to increase
over the breeding season in both sexes, although the increase was significant only in females. The new nest of remated males
was closer to their previous territory (mean 6 SE, 46 6 8 m) than that of the remated females (289 6 57 m, p , .001).
Hatching success of new nests was not different between remated males and females. Our results demonstrate that the remating
opportunities are different for male and female Kentish plovers and these opportunities vary over the season. We propose that
the remating opportunities were influenced by the male-biased adult sex ratio and the seasonal decrease in the number of
breeders. However, we stress that measuring remating times is a more direct measure of mating opportunities than calculating
the operational sex ratio. Key words: Charadrius alexandrinus, Kentish plover, mate removal, mating opportunity, offspring
desertion, operational sex ratio, parental care. [Behav Ecol 10:185–190 (1999)]
T
he evolution of parental care is often explained by the
relative magnitude of two benefits (Carlisle, 1982; Lazarus, 1990; Maynard-Smith, 1977). One benefit is derived
from the reproductive value of the offspring and is affected
by the provision of care. Thus, if parents improve the survival
chances of their offspring (e.g., by feeding them or protecting
them from predators), then parents may increase their reproductive success by caring for their offspring until their young
became fully independent. This benefit should be traded off
against the benefit of deserting the offspring. If desertion confers advantages over staying with the brood such as by allowing
an extra reproductive bout for the parent or by enhancing
the parents’ prospects for survival until future breeding seasons, then parents may desert before their offspring are independent (reviewed by Clutton-Brock, 1991; Székely et al.,
1996).
The payoffs for caring and for deserting may be different
for the two sexes. First, the value of care may differ between
males and females. For example, in many passerines only females have brood patches, so incubation by the female is
more valuable than incubation by the male. Second, males
and females may have different payoffs from deserting. For
example, if the operational sex ratio (OSR; Emlen and Oring,
1977), the ratio of available females to available males, is biased, then one sex has a higher chance of remating and reproducing than the other. The payoff from deserting may also
vary over the breeding season. For example, the OSR may
fluctuate because of different arrival times of males and females to the breeding ground. Also, if breeding is seasonal,
Address correspondence to T. Székely, Centre for Behavioural Biology, School of Biological Sciences, University of Bristol, Woodland
Road, Bristol, BS8 1UG, UK. E-mail: [email protected].
Received 18 January 1998; accepted 29 September 1998.
q 1999 International Society for Behavioral Ecology
then as the end of the season approaches, the chance of successfully completing a new breeding attempt should diminish.
Although theoretical studies have pointed out that understanding these payoffs is crucial for revealing why parents care
for their offspring (Balshine-Earn and Earn, 1997; Lazarus,
1990; Maynard Smith, 1977), empirical studies are scarce (reviewed by Clutton-Brock, 1991; Balshine-Earn, 1995; Székely
et al., 1996). Simple observation of the behavior of parents
(whether they care or desert) and estimates of their subsequent reproductive success are not sufficient because such behavior may be confounded by the individual qualities of parents. For example, those parents that provide better than average quality of care for their offspring may be more willing
to stay with their offspring, and offspring of such parents may
have a better than average chance of fledging. Furthermore,
these payoffs should be obtained from a species in which offspring desertion is part of a natural breeding strategy (Clutton-Brock, 1991). Finally, these payoffs should be estimated in
the environment where the different patterns of parental care
emerge naturally.
We investigated one such appropriate species, the Kentish
plover Charadrius alexandrinus. The Kentish plover has a variable parental care pattern—after the eggs hatch, either the
male or the female parent often deserts the brood (Fraga and
Amat, 1996; Lessells, 1984; Paton, 1995; Warriner et al., 1986).
Their mating pattern is also variable; both sequential polygyny
and polyandry occur because after desertion males and females may remate and renest. At least 37% and 27% of deserting females remated in California and in Hungary, respectively (Székely and Williams, 1995; Warriner et al., 1986).
Therefore, a major benefit of desertion appears to be reproduction in the year of desertion. The aim of our study was to
quantify the remating opportunity and the reproductive success of a deserting parent. In particular, we investigated whether the benefit of desertion is different for males and females
186
and whether this benefit varies over the breeding season. In
a companion study we analyze the payoffs from provision of
care (Székely and Cuthill, this issue).
METHODS
Experimental manipulation
Field work was carried out at Tuzla Lake (368439 N, 358039 E),
2 km south of Tuzla village in the Çukurova Delta, southern
Turkey. Approximately 1000 pairs of Kentish plovers breed
there. The experiment was carried out on the north side of
the lake in an area of approximately 1.5 km2. This site was
distinct from site B used in our companion experiment on
the value of care (Székely and Cuthill, this issue) and overlapped with site A, although a bird, nest, or brood was involved only in one of the two experiments. The study site was
a saltmarsh bordered by arable land to the north and the lake
to the south. Halophytes such as Salicornia europaea and Sueda prostrata were the most common plants (Uzun et al., 1995).
Both parents were caught on their nest between 16 April
and 16 June 1996 (n 5 40 pairs). Body mass and tarsus length
of each parent were measured, and birds were ringed with an
individual combination of color rings. We scored the amount
of intrafurcular fat using the method of Helms and Drury
(1960). One parent was released in each pair (released-1),
whereas the other parent was taken into captivity. For each
pair of nests we randomized whether the male or the female
parent was released. Before a parent was released, its clutch
was taken away and the size of the eggs was measured. We
estimated the number of days that these eggs had been incubated by floating the eggs in lukewarm water (Kis J and
Székely T, unpublished data). Only nests with three eggs
(modal clutch size) were manipulated. The eggs were distributed into other nests that were not included in this study. The
experiment was licensed by the Turkish Ministry for Natural
Parks in a location where Kentish plovers are abundant (Magnin and Yarar, 1997).
After the released-1 plovers remated or had not been seen
at the study site for at least 1 week, their previous mate was
released from captivity (released-2). We also investigated the
remating behavior of these plovers. One female, which was
released from captivity 7 days after her mate was not seen on
his territory, found her previous mate. This pair was excluded
from all analyses of remated birds.
We searched for released plovers every day until 30 June
1996. The searched area extended farther east and west than
the core where the manipulations took place, and we regularly
covered approximately 3.5 km2. Once a bird was found, we
recorded its behavior and identified whether the bird had
remated. A bird was considered remated if the courtship of a
male was accepted by a female; that is, a female followed a
male and they prepared a nest-scrape or copulated. In 1 out
of 28 remated plovers the pair-bond was not permanent, giving 27 remated birds. In addition, seven plovers were not observed to remate, although we found their new nest. The maximum remating time was assumed for these plovers (i.e., we
assumed that they found a mate the day before the first egg
had been laid for the new nest). New clutches were checked
at least every other day and daily around the expected date
of hatching. Successful clutches hatched at least one chick.
Three females were observed only once after 22, 37, and 52
days of release, when these females appeared to be single.
These observations were excluded from the analyses of remating times, as they were more than 4 SDs away from the
mean of the female population.
We aimed at recording the behavior of parents three times
each before they remated and after they remated. No data
Behavioral Ecology Vol. 10 No. 2
were collected after the new nest of remated plovers was completed. During a behavioral sample, we scanned the behavior
of the focal plover and its mate (if mated) every 20 s for 30
min. A variety of behaviors were recorded. Here we focus on
those that relate to display behavior (courtship, scraping nestscrape, and fighting with other Kentish plovers) and self-maintenance (pecking at a prey item and preening). The distance
between the focal parent and its previous nest (‘‘distance from
territory’’) was estimated every 5 mins.
To facilitate the recognition of experimental birds in the
field, we dyed the flanks of released birds with picric acid.
This was necessary to identify the experimental birds in the
large nonexperimental population. To check whether the dye
influenced mating behavior, two males and three females were
left undyed. Mating behavior of dyed and undyed birds was
not different: two undyed males stayed single for 15 and 22
days (range of dyed males: 1–52 days, n 5 28 males), and an
undyed female stayed single for 3 days (range of dyed females:
0–13 days, n 5 22 females).
Data processing and statistical analyses
We calculated volumes of completed clutches using a specific
egg-shape index for the Kentish plover (Székely et al., 1994).
Body mass was related to the intrafurcular fat score at the time
of manipulation in females (Pearson correlation, r 5 .324, p
5 .041, n 5 40), but not in males (r 5 2.116, p 5 .482, n 5
39). Behavioral variables were arcsine square-root transformed, and distance data were log10(x 1 1) transformed. Behavioral units were the proportion of time out of all observations when the focal bird was in view. Behavior of released1 and released-2 plovers was not different (two-way MANOVA,
type of release: Wilk’s l 5 0.929, p 5 .793; sex: l 5 0.672, p
5 .025; interaction: l 5 0.732, p 5 .072). Because some of
the behavioral variables violated the assumptions of parametric tests, we also investigated them by nonparametric statistics.
Nonsignificant interaction terms (p . .05) in two-way ANOVAs and MANOVAs are not reported.
Date of remating was defined as the mean date between the
date a plover was seen single and the first date it was with a
new mate. Remating time was the difference between date of
release and date of remating. Remating times were ln(x 1 1)
transformed and analyzed by parametric tests. These analyses,
however, did not take into account birds that did not remate.
Therefore, we also calculated the remating time of the sexes
using survival analyses (Norušis, 1994) and refer to these estimates as expected remating times. In the latter analyses the
terminal event (outcome) was the occurrence of remating defined as the first observation when a plover was seen with a
new mate. Several individuals did not find a new mate when
we saw them for the last time, and we treated these observations as censored (Norušis, 1994). The proportion of censored observations did not differ between males (13 out of
32) and females (12 out of 27, x2 test with continuity correction, x2 5 0.001, p 5 .975). D (which follows a x2 distribution)
and probability of Lee-Desu tests are given for the survival
analyses (Norušis, 1994). Median remating time is the time
when 50% of single birds are expected to pair. We used Cox
regression to investigate the effect of date of release on remating time (Norušis, 1994). For the latter analyses we give B
of the cumulative survival function and its significance (Norušis, 1994). Note that when B is negative, then remating
times increase over the season. The effects of date of release
(covariate) and sex of parent (factor) on remating time was
investigated by a Cox regression model in which we also included the interaction between the factor and the covariate.
Slopes of two or more regression equations were compared
by full models of ANOVAs in which remating time was the
Székely et al. • Remating opportunities in Kentish plover
187
Table 1
Behavior of single and remated plovers
Mean 6 SE % of time
Male
a
Female
Za
p
Single
Courting
Scraping
Fighting
Feeding
Preening
No. of birds
3.65
2.44
3.38
8.71
5.44
19
6
6
6
6
6
1.03
1.03
1.80
1.73
1.23
0.23
0.00
0.12
9.91
1.28
5
6
6
6
6
6
0.23
0.00
0.12
3.07
0.65
2.029
1.694
1.785
0.462
1.898
.043
.090
.074
.644
.058
Remated
Courting
Scraping
Fighting
Feeding
Preening
No. of birds
6.03
11.29
1.40
2.18
6.71
7
6
6
6
6
6
2.62
4.59
0.33
0.71
2.15
0.14
0.95
0.07
9.02
1.81
8
6
6
6
6
6
0.14
0.85
0.07
2.43
0.64
2.950
2.008
2.950
2.323
1.532
.003
.045
.003
.020
.126
Z value and probability from Mann-Whitney U test.
dependent variable, sex was the factor, and tarsus length and
body condition, or the amount of intrafurcular fat were the
independent variables. For these ANOVAs the significance of
the interaction terms between the factor and the independent
variables are given. Dates are given as number of days since 1
March. Two-tailed probabilities and means 6 SEs are given
unless otherwise indicated. We used SPSS for the Macintosh
4.0, SPSS for Windows 6.1, and MINITAB (1995) 10.1 for Windows for data processing.
RESULTS
At manipulation
We found no difference between male-released and female-released pairs in volume and in laying date of removed clutches
(t tests, p 5 .310 and .762, respectively), nor in the number of
days they had been incubating their clutch (t test, p 5 .276).
Furthermore, male-released and female-released pairs were not
different in body mass (two-way ANOVAs, male-released versus
female-released: F1,76 5 0.896, p 5 .347, sex: F1,76 5 0.061, p 5
.805), fat reserves (male-released versus female-released: F1,75 5
0.519, p 5 .473, sex: F1,75 5 1.999, p 5 .161), or in tarsus length
(male-released versus female-released: F1,76 5 0.985, p 5 .324,
sex: F1,76 5 28.260, p , .001). Finally, neither body mass nor
fat reserves of males and females were different in released-1
(t tests, p 5 .653 and .143, respectively) and in released-2 birds
(p 5 .779 and .736, respectively), but males were larger than
females in terms of their tarsus length (t tests, released-1: t 5
3.29, p 5 .002, released-2: t 5 3.52, p 5 .002).
Release from captivity
Thirteen males and 10 females were released from captivity
before or on 16 June. Males and females were released from
captivity 79.6 6 4.7 days and 87.6 6 3.9 days after 1 March,
respectively (t test, t 5 1.25, p 5 .225). Males spent less time
in captivity (13.3 6 1.9 days) than females (23.8 6 4.2 days, t
5 2.27, p 5 .041) because their previous mate paired more
quickly than the previous mates of females (see below).
Behavior of males and females
The transition from single to remated did not significantly
influence the behavior of males and females, but the behavior
Figure 1
Distance of single and remated plovers from their previous territory
(means 6 SE). The number of individuals is shown above each bar.
of sexes was clearly different (two-way MANOVA, remated status: l 5 0.776, p 5 .144; sex: l 5 0.534, p , .001). In particular, males spent more time courting (two-way ANOVAs with
sex and remated status, sex: F1,35 5 16.032, p , .001), scraping
(F1,35 5 9.981, p 5 .003), fighting (F1,35 5 5.947, p 5 .020),
and preening (F1,35 5 5.819, p 5 .021) than females. On the
other hand, females tended to spend more time feeding than
males (F1,35 5 4.093, p 5 .051, Table 1). The behavior of males
and females was unrelated to the time in the breeding season
(Pearson correlations, males: r 5 2.353–.064, p 5 .077–0.927,
n 5 26, females: r 5 2.421–.256, p 5 .152–.871, n 5 13).
Single males and females were observed at similar distances
from their previous territory (Figure 1; Mann-Whitney U test,
Z 5 1.512, p 5 .131), whereas remated males stayed nearer
to their previous territory than remated females (Figure 1; t
test, t 5 5.99, p , .001). A significant interaction between sex
and remated status indicated that females moved to the territory of their new mate, whereas new mates of remated males
moved to the territory of their males (two-way ANOVA, sex:
F1,30 5 8.836, p 5 .006; mated status: F1,30 5 1.429, p 5 .241;
interaction: F1,30 5 10.737, p 5 .003).
Time to remate
Females remated more quickly (median 5 1.5 days, range:
0.5–6.5 days, n 5 15) than males (median 5 12.0 days, range:
3.0–47.5 days, n 5 19, t 5 7.39, p , .001; Figure 2). Remating
times remained different between males and females after excluding six males and one female for which remating times
were estimated (see Methods; t 5 6.25, p , .001). Captivity
did not influence remating times, as released-2 plovers took
as much time to remate as released-1 plovers (two-way ANOVA, release type: F1,30 5 0.776, p 5 .385; sex: F1,30 5 53.973, p
, .001).
These analyses, however, do not take into account that several plovers remained single when they were observed for the
last time in the season. By using survival analyses we found
that the expected remating times of females (median 5 5.3
days, n 5 27 females) remained significantly less than that of
the males (median 5 25.4 days, n 5 32 males, D 5 15.382, p
, .0001; Figure 3). The expected remating times tended to
increase over the season in both sexes, although it was significant only in females (Cox regression, B 5 20.028, n 5 23
Behavioral Ecology Vol. 10 No. 2
188
Figure 2
Box-plots of remating time of male and female Kentish plovers. The
line is drawn across the median, the bottom and the top of the box
are lower (Q1) and upper quartiles (Q3), respectively. The whiskers
extend from the lower and the upper quartiles to the lowest and
highest observation, respectively, within the range defined by Q1 2
1.5*(Q3 2 Q1) and Q3 1 1.5*(Q3 2 Q1) (MINITAB, 1995).
Figure 3
Proportion of Kentish plovers remaining single. Plovers were
released on day 0.
plovers was similar across two populations (Portugal: 2.5 6 0.4
days, Székely, 1996; Turkey: 2.3 6 0.5 days, Mann-Whitney U
test, Z 5 0.713, p 5 .476), and it is consistent with the remating time of naturally deserting females (Hungary: 2.0 6
0.6 days; Székely and Williams, 1995). Thus females do not
seem to have difficulty in pairing. However, male remating
times appear to be different among populations because
males took less time to remate in Portugal (7.5 6 1.4 days)
than in Turkey (19.7 6 3.3 days, Mann-Whitney U test, Z 5
1.974, p 5 .048). One explanation for the observed difference
in male remating times may be related to population density.
In Portugal the breeding density is higher (5–16 nests/ha;
Székely and Williams, 1995) than in Turkey (2–6 nests/ha;
Székely T, unpublished data), so the number of females that
are willing to breed may be higher too. Future studies on
remating opportunities and population densities will be helpful to investigate the generality of the presumed relation between remating times of males and breeding density.
The OSR appears to be biased toward males in all populations
of Kentish plovers, and there may be two reasons for this putative
bias. First, the adult sex ratio may be skewed; that is, there are
more males than females capable of reproducing in the popu-
females, p 5 .044), not in males (B 5 20.017, n 5 29 males,
p 5 .343). Thus the expected remating times followed the
same trend in both sexes (Cox regression, interaction between sex and date of release: B 5 20.007, n 5 52, p 5 .543).
Remating times were unrelated to body size (as measured
by tarsus length) and body condition, both in males (multiple
regression with the remating time as dependent variable, tarsus: b 5 4.492, p 5 .587; condition: b 5 0.391, p 5 .874, n 5
19) and in females (tarsus: b 5 21.380, p 5 .879; condition:
b 5 1.004, p 5 .489, n 5 15). The slopes of regression equations were not different between males and females (ANCOVA, tarsus and sex interaction: F1,28 5 0.19, p 5 .663; condition
and sex interaction: F3,28 5 0.05, p 5 .828). Finally, remating
times were unrelated to intrafurcular fat scores both in males
(b 5 0.095, p 5 .719, n 5 18) and in females (b 5 20.247,
p 5 .169, n 5 15), and the slopes of regression equations were
not different between males and females (ANCOVA, fat and
sex interaction: F1,29 5 1.18, p 5 .285).
Hatching success of new nests
Females completed their new clutch sooner from the time of
release than new female mates of males (Table 2). However,
clutch size, volume of clutch, and hatching success were not
different between released females and new mates of released
males (Table 2). The number of chicks produced by a clutch
was unrelated to date of egg laying (Spearman rank correlation, males: rs 5 0.176, p 5 .566, n 5 13; females: rs 5 2.181,
p 5 .617, n 5 10).
Table 2
Hatching success of remated plovers with their new mate
Mean 6 SE
DISCUSSION
Clutch
No. of clutches
Completion (days)
Size
Volume (cm3)
No. of chicks
hatched/nest
No. of successful/
total clutches
Sex differences in mating opportunities
Mating opportunities were different for male and female Kentish plovers, as females took less time to find a new mate and
complete a new clutch than males. These results are consistent with previous experiments in Kentish plovers which
showed that males took more time to find a new mate than
females (Székely, 1996). Experiments have also shown that single males took longer to complete a new clutch than a pair
would normally need to replace a failed clutch, whereas single
females took no longer than pairs (Lessells, 1983). The remating time of experimentally induced single female Kentish
a
Male
Female
t/Z
p
13
22.9 6 2.5
2.9 6 0.1
23.9 6 0.7
10
13.9 6 2.0
2.8 6 0.1
23.3 6 1.3
2.65a
0.85b
0.42a
.015
.396
.682
1.5 6 0.4
0.7 6 0.4
1.46b
.146
8/13
3/10
t test and associated probability.
Z value and probability from Mann-Whitney U test.
c
Fisher’s Exact test.
b
.214c
Székely et al. • Remating opportunities in Kentish plover
lation. This explanation is in line with the findings of P. E. Jönsson (personal communication) that there were consistently more
males than females in a small breeding population of Kentish
plovers during a 10-year study in Sweden. Also, Warriner et al.
(1986) estimated that in their population of snowy plovers (C.
alexandrinus nivosus) the ratio of adult males to females was 1.4:
1. There may be several explanations for the skewed sex ratio
(different primary and secondary sex ratios, mortalities, ages at
maturation, or migration schedules between sexes), although the
exact reason has not been deduced. Second, more females may
be unavailable for breeding than males because they are incubating or attending their young, for example. The latter explanation, however, is unlikely, because both sexes incubate in Kentish plover, and after the chicks hatch, the female parent deserts
the young more often than the male.
Given the large difference in mating time between the sexes, it is surprising that some males take the risk of deserting
their brood and attempting to attract a new mate (Fraga and
Amat, 1996; Székely and Lessells, 1993). Brood desertion by
males often occurs early in the season (Székely and Lessells,
1993), which suggests that these males try to breed. The large
variation in male remating times found in our study suggests
that some males are apparently better at remating than others.
These males may be more attractive to females or better at
fighting for a mate and territory than other males. Experimental manipulations of males and their territories are required to separate these explanations.
We also found that remating time tended to increase over
the breeding season in both sexes, and we suggest two explanations for this trend. First, if the abundance of food declines
during the breeding season (Székely and Cuthill, this issue),
then deserting parents have to spend more time reaching a
condition in which they can initiate breeding. Second, the
number of single plovers that are ready to breed may decrease
over the season, so parents have to spend more time searching
for a new mate near the end of the season. This may be because the proportion of birds willing to breed decreases as the
value of reproduction (i.e., fledging success of the young) decreases toward the end of the season (Székely and Cuthill, this
issue). The duration of the breeding season may influence the
observed mating patterns. For instance, in many Arctic birds
the breeding season is short, which allows only one breeding
attempt (Gratto-Trevor, 1991). However, when a breeding season was exceptionally long, female dunlins Calidris alpina had
time to mate with new males and renest (Soikkeli, 1967).
Benefits of desertion
Deserting animals may derive other benefits than remating
(reviewed by Clutton-Brock, 1991; Székely et al., 1996). First,
desertion may occur when the incubating parent is in a poor
condition and thus terminating care may increase the parent’s
chance of surviving. For example, incubating penguins and
seabirds often abort nesting when their body condition is poor
(Chaurand and Weimerskirch, 1994; Olsson, 1997; Yorio and
Boersma, 1994). Second, parents may also terminate care late
in the season when they have to prepare for the nonbreeding
period by moulting, for example (Urano, 1992).
Theoretical analyses are invaluable for separating the effects of the various benefits of desertion. In a single-sex model
of avian parental care, Webb et al. (submitted) investigated
the expected behavior of a parent in relation to its state (body
reserves) and time in the breeding season. This theoretical
study found that parents with low body reserves deserted because the continuation of care would risk their survival. This
decision occurred at any time during the breeding season.
However, parents with high body reserves early in the season
also deserted, although these parents were not threatened by
189
starvation. Rather, these parents searched for a new mate and
attempted to breed again. Finally, some parents deserted at
the end of the breeding season when the value of their current offspring was outweighed by the influence of care on
their own chances of the surviving the nonbreeding season.
Separation of these different reasons for desertion require experimental manipulation of the state of the parent at different
times in the season.
The significance of mating opportunity for the evolution of
parental care
Understanding mating opportunities may be important for
three reasons. First, the option to breed again may influence
the duration and intensity of parental care. For example, male
cichlid fishes are more likely to terminate care when their mating opportunity is high (Balshine-Earn, 1995; Balshine-Earn
and Earn, 1998; Keenleyside, 1983). Similarly, male zebra finches Taeniopygia guttata invest less in their offspring if they have
better than average chances of mating and reproducing again
(Burley, 1988), and parental care by male red-winged blackbirds Agelaius phoeniceus was reduced when the male had access to a fertile female (Whittingham, 1994). Second, mating
opportunities may influence the observed mating patterns. For
example, if a male has no chance of attracting another female
(because the breeding season is short, the OSR is male biased,
or the male is of poor quality), then he may do better by guarding his mate and attending his first female’s brood than wasting
time and energy on courting females in vain. This has been
experimentally demonstrated in insects and in fish (BalshineEarn, 1995; Vepsalainen and Savolainen, 1995). Third, mating
opportunity, in particular the OSR, has been proposed to have
a major influence on the intensity of sexual selection and competition for mates (Andersson, 1994; Emlen and Oring, 1977;
Kvarnemo and Ahnesjö, 1996). When the OSR deviates from
unity, the intensity of mating competition is expected to increase (Colwell and Oring, 1988; Gwynne, 1990; Parker and
Simmons, 1996).
Although OSR has often been used as an index of mating
opportunity, this relation may not always be correct. First, in
many animals it is not straightforward to assess whether an
animal is in breeding condition without internal examination.
Even in those species in which it is relatively easy to distinguish breeders from nonbreeders, there is a possibility that
the animals may not perceive their population members the
same way (breeder versus nonbreeder) as the researchers do.
Second, the OSR represents only a ratio, and the mating opportunity should depend on the density of males and females
in a population as well, because the animals have to find the
available individuals. Therefore, a more realistic index of mating opportunity should depend on the absolute number of
males and females in the population (Webb et al., submitted).
We believe that the experimental assessment of mating opportunities is preferable over simply sampling the animals in
a population and deriving their OSR because our measurements such as mating times and reproductive success are
based on the responses of the animals.
The observed bias in remating opportunity between males
and females in our study may have an implication for the
evolution of polyandry (Oring, 1986; Székely, 1996). Classical
polyandry (i.e., when a female lays separate clutches for several males in a breeding season) is a rare mating system in
birds; the best-known examples are in shorebirds (CluttonBrock, 1991; Oring, 1986). We propose that the high remating
opportunity for deserting females may facilitate the evolution
of polyandry. This needs to be investigated by experimental
studies of remating opportunities in other shorebird species
in which polyandry is facultative. However, the initially male-
190
biased OSR may change over evolutionary time as a result of
a response by female shorebirds, such as brood desertion. For
example, the proportion of females deserting may increase in
the population. Also, females may start to desert their nest
and mate at a younger offspring age, such as shortly after egg
laying or during incubation (Reynolds and Székely, 1997). In
addition, females may compete to return to the breeding
ground at an earlier date to secure a mate or a breeding territory (Colwell and Oring, 1988; Reynolds et al., 1986). Taken
together, the results of these processes may be that the observed OSR in contemporary populations of polyandrous
shorebirds may be equal or female-biased, although the initial
condition for the evolution of female desertion and polyandry
might have been a male-biased OSR.
In conclusion, we have demonstrated experimentally that female Kentish plovers have better remating opportunities than
males. This result is consistent with previous experiments on
the Kentish plover. It is also consistent with the observed frequencies of desertion; that is, females desert their brood more
often than males in all populations that have been studied so
far. We propose that the male-biased OSR is due to a malebiased adult sex ratio and encourage researchers to gather data
(which are comparable to our study) in other species. The significance of mating opportunity is that it links mating patterns
to parental care. Although this link has been implicitly assumed, it is not fully understood either theoretically or empirically. In particular, we propose that a male-biased OSR facilitated the evolution of polyandry, although, due to a response
by female birds to the favorable mating opportunity, the OSR
may well be significantly shifted through evolutionary time.
Thus the links among observed patterns of parental care, mating system, and OSR may not be as simple as the impression
pioneering papers (e.g., Emlen and Oring, 1977) have created.
The project was funded by a Leverhulme Trust grant to A. I. Houston,
I.C.C., and J. M. McNamara (F/182/AP) and by an Országos Tudományos Kutatási Alap grant to T.S. (T020036). T.S. was also supported
by a Natural Environment Research Council grant to A. I. Houston,
I.C.C., and J. M. McNamara (GR3/10957). Rings were provided by P.
R. Evans (Durham University) and Radolfzell Vögelwarte, Germany.
Ö. Karabaçak (Milli Parklar, Adana), M. Yarar (DHKD, Istanbul), G.
Sarigül (DHKD, Tasucu), and V. van den Berk (National Reference
Centre for Nature, Wageningen) helped us by providing practical information over the duration of the field study. We thank A. I. Houston
and two referees for their comments on the manuscript.
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