COPULATIONSDESPITELOWFREQUENT
IN WHITESTORKSCOMPETITION(CICONIA

SPERM

CICONIA)by

FRANCISCO S. TORTOSA1) and TOMAS REDONDO2,3,4)(1 Departamento de Biologia Animal, Facultad de Ciencias, Universidad de Córdoba,
E-14071 Córdoba, Spain and 2 Estación Biológia de Doñana, CSIC, Apdo. 1056, E-41080
Sevilla, Spain)(With6 Figures)(Acc.1-VI-1992)

Summary
White Storks Ciconiaciconiapaired for ca. 30 days before laying a clutch. During this period,
mates copulated frequently (160 copulations/pair; 0.4 copulations/daylight h), but copulation rate was drastically reduced a week before laying of the eggs. Both fewer copulation
attempts by males and lower female receptivity accounted for this reduction. This pattern
was the same regardless of whether pairs nested solitarily or in colonies. Colonial as well as
solitary males spent more time at the nest before egg-laying while the opposite trend wasfound for females. Consequently, females were more likely to remain alone at their nests
while ovulating. Colonial birds had ample opportunities for engaging in extra-pair copulations (EPC) during the female fertile period, but these were very infrequent (0.4% of all
copulations) and involved recently-paired birds exclusively. This suggests thatsuccessful
spermcompetition in this species is of little relevance for explaining patterns of pair
copulations. Accordingly, males did not guard their female mate and the timing of copulation was poorly tuned to chances of fertilizing the female's eggs. However, it remains to be
explained why storks copulated so much and for a prolonged period when the risk of EPC
was so low. It is suggested that copulations may be part of a signalling system by whichmales advertise and females assess the physical condition of the male, which is likely tocorrelate with the ability of males to forage efficiently for them and their offspring. In
support of this possibility, males who copulated frequently fed chicks at a higher rate during
the nestling period.
3) Present address: Department of Zoology, University of Cambridge, Downing Street,
Cambridge CB2 3EJ, UK.
F. ALVAREZ, AMAT,
T. BIRKHEAD,
C. DELECOURT,B.
4) We are grateful to E. AGUILERA,J.
A. LOTEM,
A. MOLLER, J.
NEGROand an anonymous referee for
ENS,R. FRAGA,K. LESSELLS,
for translating the summary. This
many helpful suggestions and criticisms, and to J. KRAUSE
research was made possible by funds provided by Junta de Andalucia (groups 4004 and4005) and CYCIT research project PB87-0316, and by a postdoc MEC grant (Perfeccionamiento de Doctores y Tecnologos en España) and a Fleming British Council/MEC fellowship to T. R.

289
Introduction
Many birds and mammals copulate far more frequently than is needed forfemales. Copulations
entail costs,
successfully
inseminating
probably
vulnerable
to predation
making partners(BIRKHEAD et al., 1987), andconsume time and energy that otherwise could be spent for other purposes (PARKER, 1974; DALY, 1978; DEWSBURY, 1982), thus copulation
selection favouring low
patterns are expected to evolve under directional
rates (EATON, 1978). However,birds show a
copulation
monogamous
remarkablevariation in the extent and duration of copulainterspecifiction periods, which suggests that copulation
behaviour
is under more
selectionthanthefemale's eggs
complexpressures
merely fertilizing
et(BIRKHEAD al., 1987; DEWSBURY, 1988).
BIRKHEAD et al. (1987) looked for an adaptive
for this
explanation
variationand found that neither fertilization
constraints
nor predationpressures could satisfactorily
explain it. Instead, they concluded that theextent to which the female is likely to be fertilized by nonmate males (i.e.
the intensity of sperm competition(PARKER, 1970) among ejaculates)
determines how frequently a male should copulate with his female mate inorder to be certain of his paternity(BIRKHEAD et al., 1987; BIRKHEAD,
MOLLER&1988;
BIRKHEAD, 1992). Extra-pair copulations (EPC) are widein
birds
spread(see reviews by GLADSTONE, 1979; FORD, 1983; McKINNEY
et al., 1983, 1984; MocK & FuJIOKA, 1990; WESTNEAT et al., 1990;
BIRKHEAD & MOLLER, 1992), and recent methodologicalinadvancesforinbroodsoftechniques
detectingmultiplepaternity
apparently
that EPC sometimes lead to amonogamous
species have demonstrated
high incidence of extra-pair fertilizations(MocK & FuJIOKA, 1990; WESTNEAT et al., 1990; MOLLER, 1991; WEATHERHEAD & MONTGOMERIE, 1991).).
When males make a substantial investment in offspring care, as in mostbirds, they will obviously benefit from fertilizing the eggs ofmonogamous
nonmate females, thus parasitizing
the paternal expenditureof cuckolded
males. Females could also benefit from copulating with several males in aseason (WESTNEAT et al., 1990; BIRKHEAD & MOLLER,
given breeding
males will be expected to actively seek copulations
1992). Consequently,
with nonmate females, trying simultaneously
to protect their own patertheirfemalemate
while
she is fertile), and restrict
nity (e.g. by guarding
their parental expenditure
to the offspring of their mate. On the other
hand, the female should try to maintain a stable pair bond with her matein order to benefit from his paternal
while occassionallyexpenditurenonmatemales
tofertilize
herThisratherallowing
eggs.
complex sce-

290
nario in which both members of a pair practise a mixture of monogamy
and promiscuity
was termed by TRIVERS (1972) a Mixed Reproducctive
andboththeoretical and empirical evidence suggest that it may
Strategy,
be common, rather than an exception, among birds traditionallyconsidered to be exclusively monogamous(FORD, 1983; McKINNEY et al., 1984;
BIRKHEAD et al., 1987; MOCK & FUJIOKA, 1990; WESTNEAT et al., 1990).
EPC rates vary both across populationsof a species (MCRoBERTS, 1973;
MINEAU & COOKE, 1979; WERSCHKUL, 1982; FREDERICK, 1987; SMITH,
1988; MCKILLIGAN, 1990) and among related species (BIRKHEAD, 1978;
MCKINNEY et al., 1983; LEFELAAR & ROBERTSON, 1984), but the causessuch variation remain poorly understood.
However, two facunderlying
tors are thought to facilitate the occurence of EPC:
1) A high density of breeding pairs, like colonial nesting (FORD, 1983;
WESTNEAT et al., 1990). Althoughis neither necessary nor
coloniality
ansufficient for
EPC strategy to occur (WESTNEAT, 1987), some studies(BIRKHEAD, 1978; MOLLER, 1985, 1987a) have reported EPC to be moreprevalent among colonial than among dispersed or solitary breeders.
2) The lack of effective mate guarding by males (BIRKHEAD et al., 1987;
MOLLER & BIRKHEAD, 1992). Many birds of prey (including owls andshrikes) cannot effectively guard their female mate during her fertile
period, because males have to hunt to provision the female, and thiswould render females especially suceptible
to EPC attempts by othermales. Similarly, males of colonial herons, egrets, and ibises also cannot
guard their female mate because they can only leave the nest to forage
when it is guarded by his mate, in order to prevent nest destruction
byconspecifics(FUJIOKA & YAMAGISHI, 1981). These species are actually
among the best known examples of the existence of a Mixed Reproductive
Strategy (GLADSTONE, 1979; FUJIOKA & YAMAGISHI, 1981; WERSCHKUL,
1982; FREDERICK, 1987; AGUILERA & ALVAREZ, 1989; MCKILLIGAN,
1990).
Some colonial storks (Ciconiidae) fall within category 2) above. Nests areoften highly clumped(HAVERSCHMIDT, 1949; KAHL, 1966a, b, 1972;
CRAMP & SIMMONS, 1977; CREUTZ, 1985) and stealing of nest material is
Detailed
information
on mating behaviour
and copulation
frequent.
rates is lacking for virtually all species but preliminary
observations
rates
suggest that white storks Ciconia ciconia have high copulation
hence
a
of
was
assumed(CREUTZ, 1985),
high degree
sperm competition
for this species (BIRKHEAD et al., 1987; MOLLER & BIRKHEAD, 1992). This
paper reports the results of a study originally aimed at recording variation
in intra- and extra-pairof white storks nesting at
copulation
patterns

291
different

densities.

We also found
to expectations,rates.
extremely high pair-copulation
we found EPC to be rare and unlikely
However, contrary
so we consider copulation patterns into result in extra-pair fertilizations,
to arise from selection
thanthis species
otherpressures
sperm
competition.
Methods
Breeding data were collected during November 1989 to July 1990 and November 1990 toJuly 1991, covering the whole breeding cycle from pair settlement at breeding sites tofledgling independence. Observations were performed at four different breeding sites insouthwestern Spain. Information concerning the year when data were collected, observation hours and sample sizes is presented in Table 1. Some birds were marked withnumbered PVC rings (see below). Among unmarked birds, some could be recognized by
distinctive features: abnormal bill colouration (I bird), large permanent callosities at thetibio-tarsal joint (3 birds), and the unique pattern of distribution of black outer tail-feathers(27 birds) (for details of the identification method see CHOZAS,1983). The remaining birds
were marked with permanent non-toxic dye.
I. La Dehesa Colony. The largest breeding colony in ·Vestern Europe, comprising morethan 100 pairs nesting on a white olive tree Olea europaeawoodland near rice fields. A
regular banding program with numbered PVC rings has been routinely performed since
1985, hence most birds younger than 6 years old were marked. We selected 23 pairs nestingin the densest part of the colony as a sample for recording behavioural observations. 25
birds were ringed, 4 were dyed and 17 showed distinctive features.

TABLE 1. The number of white stork pairs observed,
per nest, nest dispersion and the type of data collectedsite during 1990 and 1991

observation
hours
for each breeding1) 1: La Dehesa; 2: Pedroche; 3: Jerez; 4: solitary nests near urban Córdoba.

292
2. Pedroche Colony. A small colony of 12 pairs nesting on buildings. No bird was ringed, 10
were dyed and 9 showed distinctive features. All birds abandoned the colony area after
breeding.
3. Jerez Colony. An 8-pair colony of sedentary wild birds nesting at Jerez Zoological
Gardens, where they live year round. 11birds were ringed and 5 showed distinctive
features.
4. Solitairy nests. Eight unmarked pairs nesting dispersed over a wide area of cultures
surrounding urban Cordoba were observed. Nests were abandoned after breeding.
The information recorded at each breeding site during a given breeding season issummarized in Table 1.
Continuous observations from dawn to dusk were performed during the earliest (prenestling) phase of the breeding cycle at all focal nests, and continued throughout thenestling period at La Dehesa and Pedroche. Observations took place from hidden places at
10-70 m from the nests with the aid of 20-45x60 zoom telescopes. Due to the general slow
movements of adult storks, it was possible to obtain a continuous sampling of behaviouralvariables by keeping under observation all focal colonial pairs simultaneously. Continuous
sampling was employed for measuring the percentage of time spent at the nest by males andfemales and the rate of occcurrence of the following behaviours: copulations (see below),food provisioning to nestlings, gathering and stealing nest materials, aggression and visits toa different nest.
Copulations between members of the same pair (Pair Copulations, PC) were consideredsuccessful if they ended in cloacal contact. Copulations in which the male mounted thefemale but no cloacal contact followed were regarded as copulation attempts, in addition tomounting attempts by the male mate. The duration of copulations was measured with astopwatch and included mounting movements. Male storks were easily dislodged from thefemale's back in very windy days, so we did not include in the sample those copulations
occurring when birds had obvious difficulties for maintaining the equilibrium due to heavy
wind.
Since female birds can store viable sperm for several days following copulation, theduration of the fertile period (i.e. the period over which copulations can result in fertilization) spans from some days before laying of the first egg to ca. 24 h before laying of the last
egg in the clutch (BIRKHEAD,
1988). The duration of sperm storage in birds is dependent
upon several factors. Species in which males and females spend relatively little time
together during the laying period (e.g.many seabirds), and species in which copulations are
infrequent (e.g. some lek-breeding galliforms) have the longest durations of sperm storage
recorded (BIRKHEAD& MOLLER,1992). For the remaining birds, the average duration of
sperm storage ranges between 6 and 11 days (average 8.6) and shows a positive correlation
with the spread of laying, i.e. the product of clutch size and the mean interval between eggs
& MOLLER,1992). We lack information about the duration of sperm storage in(BtttxHEwD
any living species of stork. Consequently, we estimated it as the predicted value for a laying& MOLLER'S
spread of 6 days (4x1.5) calculated from BIRKHEAD
survey (1992, table 3.3),
which renders an estimated duration of 8 days.The viability of stored sperm may be highly
reduced at storage durations longer than the average duration of sperm storage (BIRKHEAD& MOLLER,1992). Consequently, we will assume that the period of maximum fertilizabilityof the female (MF) lasts from 7 days before laying of the first eggs (day 0) to the day before
the last egg in the clutch is laid. Accordingly, the period preceding maximum fertilizability(pre-MF) will then referred to as the period between pair formation and day -8. In someanalyses, we also considered the period of pair formation (the 10 days following pairformation), and consequently those days were not included in the pre-MF period wheneversuch distinction is made.
We also recorded the calendar dates of settlement at the nest (migrating birds only), pairformation (the date when a pair started to copulate), and laying of the first egg. In addition,
we determined clutch size and fledging success as the number of chicks reaching nutritional

293
independence. When analyzing the relationship between brood size and fledging successwith rates of copulation and food provisioning, we only took into account those broods withno partial mortality due to causes other than starvation.
During 1991, we recorded the body mass of 9 out of the 12 breeding males at Pedroche
Colony during the female pre-MF period. Males were attracted to a portable balance
provided with a baited platform placed close to the nest, allowing the male to land on it,
while an observer remained in a hide a few metres from the balance. The value closest to
the onset of laying for each male was selected. In addition, we measured the cylindricalvolume (height x cup area) of nests before the arriving of the breeding birds.
Observations at Jerez Colony during 1991 were intended to determine the effect of
supplementary feeding upon copulation and nest attendance patterns. Birds were continuously provisioned with ad libitumamounts of horse meat from at least a month before egg
laying. Supplementary feeding at La Dehesa and Pedroche colonies was precluded becauseof the disturbing effects of daily provisioning. We compared the behaviour of males at Jerez(food-supplemented pairs in the text) with that of males at Pedroche (non-supplemented
pairs). It is unlikely that any difference between the two sites (except for the treatment)
could account for the differences observed because birds breeding at such different sites as
La Dehesa, Pedroche and Cordoba (solitary pairs) showed a very high uniform pattern of
copulations and nest attendance (see Results).
Statistical analyses were performed according to ZAR (1984). Behaviour rates werecompared by mean of two-way ANOVAs accounting for the effects of breeding site andtime in the female breeding cycle. Since the same pairs were observed throughout thenesting cycle, we used a repeated measures design (SAS Institute 1987) to guarantee
statistical independence between data points. All simple linear correlation coefficients
appearing in the text are nonparametric (Spearman).
Results
1. Pair

settlement

andformation.

Colonial
males (N=32) arrived at breedingsites and settled at nests
between
15 Novemberand 17 March (median
17 January).
Dates ofsettlement at Pedroche colony were inversely correlated with male bodymass (Spearman
r=-0.75, p<0.05, N=9). Females arrived on average 9days (±10.3 SD, N=32) later. Out of 35 pairs with known settlement
dates, males occupied first a vacant nest in 28 cases, and females in theremaining 7 cases. Those males (N=28) who settled at nests prior to theirfemale mate accepted and paired with the first incoming female, but 3 outof 7 unpaired
females occupying vacant nests repelled the first arriving
and
male,
paired with the second one.
At Pedroche, larger nests were occupied first (r=-0.83, p<0.01, N=1 1).
Males who obtained nests earlier in the season attracted mates sooner, sothat male settlement
dates were highly correlatedwith female pairing
dates (Pedroche: r=0.99, p<0.001, N= l; Solitary pairs, r=0.97, p<0.01,
N=8). Pairs formed earlier in the season tended to lay eggs earlier (Pedroche : r=0.49, N=11, ns; Solitary pairs: r=0.84, p<0.05, N=8). In turn,clutch size decreased
as the season advanced
r=-0.46,(La Dehesa:

294
p<0.05, N=23; Pedroche: r=-0.83,
p<0.01, N=12), as did the number ofthat
Dehesa:r=-0.70,
young
fledged (Lap<0.01, N=23; Pedroche: r=0.75, p<0.05, N=10).
Both members of a pair remained together for ca. 30 days before thestart of laying (La Dehesa: 29 days ± 14 SD, N=19; Pedroche: 25 days ±17 SD, N= 12;jerez:
37 days ± 15 SD, N=8). Some birds failed to attract amate (Small colonies only, 1990: 4 out of 48; 1991: 5 out of 45). Virtually
all unmated birds behaved as males, displaying at females, aggressively
the nest and actively gathering
nest materials,
which could
defendingindicate that sex ratios at breeding sites were slightly male-biased.
2. Timingof pair

copulations.

We recorded 5,850 PC attempts at colonial nests, of which 4,230 weresuccessful (72.3%). The same figures for solitary pairs were 1,065 and 805(75.6%), respectively.
Copulations
always took place on the nest, and nobird was observed to attempt copulatingout of a nest. Males solicitedthefemale'swiththeir necks. Females wereback
copulations
by stroking
never observed to display behaviours
which could be interpreted
as asolicitation. A female showed her lack of receptivity toward male copulation attempts by slightly moving away when the male attempted to mounther. Female unreceptivity
was the cause of most copulation
failures. A
complete mounting sequence ending in cloacal contact lasted on averagein mounting
12.2 s (± 1.3 SE, N=51). No differences
durations
weredetected according to breeding site or time in the female cycle.
During the pre-MF and the MF periods, white stork pairs copulated
160 times on average (SE=7.6, N=51, all pairs). Some copulations
tookplace during the incubation period, yielding a mean number of 206 (± 8.5SE) copulations
per breeding season. Both at colonial and solitary nests,
PC rates declined during the breeding cycle but not steadily, reaching apeak shortly after pair formation and showing a two-fold decrease arounda week before clutch initiation (Fig. 1). Such a seasonal decrease was dueto the combined effects of males soliciting fewer copulations
and a lower
PC ratio during the MF period (Table 2). Colonial
successful/attempted
at similar rates than solitary pairs, but colonial males
pairs copulated
more
attempted
copulations(Fig. 2, Table 2). This difference is probably
due to the higher proportionof time that colonial birds spent at the nest
rates per h the pair spent together were slightly(Fig. 2), since copulation
higher for solitary pairs (Table 2).
Colonial pairs showed a bimodal daily rhythm of PC, with peaks in295

Fig. I. Variations in the average frequency of pair copulations per daylight h of colonial(open dots) and solitary pairs (black dots) during the female breeding cycle divided into two
periods: the 10 days following pair formation (left side, day 0 = day of pair formation), andthe period preceding and following egg laying (right side, day 0 = day of laying of the firstegg in the clutch). All pairs were incubating beyond day +6.

TABLE 2. Meanvalues (SE in brackets) of pair copulation
rates, male
success (the percentage
of total
copulation
attempts, and the copulatory
male copulation
attempts
ending in cloacal contact) of colonial (LaDehesa, Pedroche) and solitary White Storks during the 10 days following(PF), and the female pre- MF (P) and MF (F) periods
pair formation

1)F values from a two-way repeated measures ANOVA assessing the effects of Coloniality
C (df =1,123), time in the female breeding cycle F (df = 2,123), and their interaction CxF(df 1,123).
* p<0.05; ** p<0.01; *** p<0.001.

296

Fig. 2. Mean (± SE) frequency of pair copulations, the percentage of daytime spent at thenest by both members of a pair, and the percentage of time that the female mate and thenest were left alone, according to female reproductive stage for colonial and solitairy pairs:
A: ten days after pair formation; P: pre-MF period; F: MF period; I: incubation; LC: largecolony; SC: small colony; SD: solitary, dispersed nests. See text for definitions.

and late afternoon
The afterearly morning (0700-0800)(1700-1800).
noon peak was especially marked during the female MF phase (Fig. 3).
Daily variations in PC rates could be the result of both males and females
actively seeking more copulations
during peaks of PC activity or, alternatively, be a side-effect of diel variations in the time both members of ato copulate duringpair spent together. White storks had little opportunity
the central daylight hours, because the pair-staying
ratio also showed abimodal daily pattern. Calculationof PC frequencies per h the pair stayed
together showed that birds actually seeked more copulations
during the
dusk hours of the female MF period (Fig. 3).
Those pairs copulating
more frequently
during the female pre-MF
also
did
so
MF
the
femalephaseduringphase (r=0.33, p<0.05, N=43, allbutPCrates during the incubation
pairs),
daily
period were not corre-

297

Fig. 3. Daily variation in the pair copulation rate per daylight h (open dots) and per h thepair stayed together (black dots) during the female pre-MF and MF periods. Differences
between hours are significant in all four cases (repeated measures ANOVA). Bars aroundmean values are SE.

lated with PC rates during the female pre-MF (r=0.02, ns, N=43), or MF
phase (r=0.09, ns, N=43).
on
for males to copulate immediately
There was a strong tendency
to
the
than
to
the
nest
site
more
expected according
frequently
returning
distributionof time that both members of a pair spent together. Males
copulated at a higher rate within the 10 min of arrival than during the restof the time both members of a pair spent together. This differed (male bytest, p<0.05).
male) from the expected values in Table 3 (Chi-squaredeviated
from
all
and
males
colonial
significantly
solitary
Virtually
expected
3. Patterns(Binomialof nesttest, p<0.001).
attendance.

at colonial and solitary nests males and females differed in thethe nest in relation to theof daylight hours spent attending
proportion
female breeding stage (Fig. 2). Results from "a posteriori" multiple comparBoth

298
TABLE 3. Observed
rates of colonial (La Dehesa, Pedpair copulationroche) and solitary males during the female pre-MF and MF periods
during the 10 min following arrival of the male at the nest and during therest of the time that both members of a pair remained together

Expected values are those estimated under the hypothesis that copulations occur uniformly
in time. Values are the mean number of copulations per h the pair stayed together and SD(in brackets) (N=51).
).

isons (Scheefe test) in repeated measures ANOVAs assessing the effects offemale breeding stage and coloniality upon percentagesof time spent at
the nest for males and females revealed the following significant trends.
Both colonial and solitary males spent less time at the nest after the end of
the female pre-MF period. Colonial males spent more time at the nestthan solitary ones at any period. Females spent a significantly
higherof daytime at the nest once they entered the MF period.
proportion
Females at solitary nests spent less time at the nest than colonial ones.
At Pedroche,heavier males spent a higher proportionof daytime attheir nests than lighter males during the female pre-MF period (r=0.71,
p<0.05, N=9). Females paired to heavier males spent less time alone at
the nest (r=-0.66,
p<0.05, N=9). In addition, fledging success was poswith the percentageof time a male spent at his nest
itively correlated
during the pre-incubation
period (r=0.48, p<0.05, N=23 colonial pairs).
Variationsin the pair-staying
ratio for colonial and solitary pairsin Fig. 2. A significant
the
are
shown
decreaseduringbreeding cycle
occurred at the onset of incubation.
In addition, solitary pairs spent alower proportionof time together at the nest than colonial ones. Since
males remainedat the nest for longer than females during the pre-MF
period, females were much more likely to be alone at the nest during their
MF period, and such a trend was the same for colonial and dispersed
nesters (Fig. 2). The percentage
of daytime that nests remained
unattended was higher for solitary than for colonial breeders and reached aminimum during the incubation
period (Fig. 2).

299
4. Stealing of nest

material.

A likely reason why at least one member of a pair should remain at thenest during most of the breeding cycle is that, at colonies, unattended
nests were soon pillaged by neighbouring
birds. In 38 focal pairs, 32 males
19
females
to steal material
andwereobservedfrom(50%)(84.2%)
nests. Out of 1,250 episodes of nest robbing, 78.7% wereneighbouring
males and 21.3% by females. In virtually all cases where abyperformed
thief attempting
to steal material if it was discovered by some member ofthe resident pair, it was attacked (N=275), 18% of such encounters endingin physical combat. Bleeding injuries were apparent in 2% of cases. Mostrobbing attempts were successful, however, and resident pairs only managed to prevent theft in 22% of cases. When both members of a resident
pair were present, males aborted robbing in 69% (± 2.0 SE) and females
in 31% (± 1.4 SE) of cases (N=43 pairs). Despite intense aggressive
defense by resident pairs, robbing attempts were directed at active, occuthan expected by chance according
to thepied nests more frequently
of
and
Of
males
at
La
nests.
Dehesa20
availability
occupiedunoccupied
colonies (where unoccupied
nests were available), 13 directed aandjerezofsignificantly higher proportion
robbing attempts towards occupied (butnests (Chi-square,
unattended)neighbourp<0.05), 2 showed a signifiand 5 did not differ from expected (Binomial test,
cantly lower proportion
p<0.01,N=15).

5. The effect of supplementaryattendance
patterns.

feeding

upon

PC

rates

and

nest

No differences in hourly PC rates were found between non-supplemented(N=12) and food-supplemented(N=8) colonial pairs, but a significant
interaction
betweentreatment
and phase in the breeding cycle
appearedless frequently(Fig. 4). Food-supplemented
pairs copulated
during thefemale pre-MF period and more frequently during the incubation
periodthan non-supplemented
The
total
numberofpairs.
copulations per clutch±
was higher for food-supplemented
SE40
as. 156 ± 10 SE) but
pairs (186the ditterence
was non significant.
Males at food-supplemented
nests
of daytime at their nests at any breeding stage
spent a higher percentage
and did not decrease attentivenessonce their female mate entered the MF
atFemales
nests also spent higher time
period.
food-supplemented
amounts at their nests than females in non-supplemented
nests (Fig. 4).

300

Fig. 4. Mean (± SE) frequency of pair copulations, the percentage of daytime spent at thenest by both members of a pair, and the percentage of time that the female mate remainedalone, according to female reproductive stage for food-supplemented pairs (FS, right side)and non-supplemented pairs (NS, left side). Explanations as in Fig. 2.
6. Correlatesof PC behaviour.

of PC and the apporThere was an association between the occcurrence
moretionment of nest material by male mates. Male storks contributed
materials.
Like
PC
rates
to
the
collection
of
nest
(Fig.
(67%) than femalesof apportionment
trips by the male decreased1), hourly frequencies
around the onset of laying (Fig. 5). The success of copulation attempts by
the male during the 10 min following arrival at the nest largely depended
Females were more likely to beon whether it carried nest materials.

301

Fig. 5. Daily rates of male trips to the nest transporting nest materials plotted against timein the female breeding cycle (day 0 is the day of laying of the first egg in the clutch). Bars
around means are SE.
after his
receptive to copulation attempts by their male mate immediately±
arrival at the nest if he brought
8.5 SE ofnest materials(83.6%
copulation
success) than if not (68.7% ± 9.2 SE) (Wilcoxon test, Z=5.2,
In addition,
male experience
with female
N=43, p<0.001).
previous
seemedtoaffectreceptivity
subsequent nest-building
activity of the male.
Males were more likely to bring nest material during the trip following a
successful copulation (26.7% ± 10 SE) than a failed copulation (23.0% ± 7
Rates of apportionmentof nesttest, Z=2.2, p<0.05).
SE) (Wilcoxon
materials by individual males were correlatedwith PC rates during thefemale pre-MF and MF periods (Table 4).
The effect of male settlement
dates upon PC rates was obscure. At
results during 1990 and 1991. The
Pedroche, we obtained contradictory
correlation
showedthese
twovariables
highbyduring the pre-MF period
in 1991 could in turn explain the relationshipbetween PC rates and nest
volume during the same year. When the effect of settlement
date wascontrolled
for, nest volume and PC rates failed to show a significant
correlation(partial r=0.52, df=8, ns). Male body mass seemed not toaffect PC rates to a great extent (Table 4) but, like with nest volume,
sample sizes were too small to be conclusive.

302
rates per daylight h obtained forof pair copulation
TABLE 4. Correlatescolonial and solitary pairs during the female pre-MF and MF periods

Values are Spearman rank correlation coefficients and sample sizes.
I) La Dehesa; 2) Pedroche.
*** p<0.001.
*** p<0.05; p<0.01;

with malerates showed a significant positive correlation
Copulation
of
time
males
at
the nest
rates
and
the
stayedchick-feeding
percentage
rate
and
rate
The
correlation
betweenchick-feeding(Table 4).
copulation
but
the
of
after
for
brood
size
effects
controlling
percentage
disappeared
time that males remainedat the nest during the pre-MF period still
rates whenwith chick-feeding
showed a significant partial correlationbrood size was kept constant (partial r=0.56, df=20, p<0.01). Fledging
with copulation
rates during the female pre-MF
success was correlatedThe
betweenfrequency and male feeding
relationshipcopulation
period.
rates was more clear when the total number of copulations per clutch wasmales fed chicks at higher
rates
considered.
Frequently
copulatingfortheeffect
of
brood
size
even
after
N=23,
controlling(r=0.59,
p<0.01)The
numberofclutchcopulations
per(partial r=0.56, df=20, p<0.01).
of time spent by males at the nest
also was correlated with the percentage
during the pre-MF period (r=0.41, N=35, p<0.05). Rates of chick provisioning by females were also significantly correlated with PC rates, after
for brood size (partial r=0.46, df=20, p<0.05). In fact, chickcontrollingrates by both members of a pair were highly correlated eachprovisioning
other (partial r=0.91, df=20, p<0.001).

303
7. Extra-pair

copulations

at colonial

nests.

forthat both males and females had ample opportunities
Despitein
EPC
behaviour
with
birds
of
the
sex
neighbouring
oppositeengagingof EPC was
during the female MF period (Table 5), the occurrence
extremely rare. The number of successful EPC was 19 (13 at La Dehesa, 6
which renders a proportionof 0.45% of total successful
at Pedroche),On
55
occassions(see below), already paired storks were
copulations.
a
nest
in
which
a member of the opposite sex stayed
observed to fly toalone but, except in the 9 cases reported, males never attempted to mountof EPC attempts as a percentage
females. This means that the proportionwould
lie between 0.32 and 0.94%,
of total copulation
attempts (5,850)
the former figure being probably more realistic.

TABLE 5. Opportunities

for EPC for colonial

males and females

Mean values and SD (in brackets) are given for the percentage of daytime a fertile female
was alone at her nest while a neighbouring male was present (opportunity for females) andthe percentage of daytime a male was present while a neighbouring fertile female was alone
at her own nest (opportunity for males).

Nine females belonging
to 43 study pairs participatedin successful
EPC. Two ringed females were 5 and 3 years old. Six females flew to, and(< 20 m) male, while the remaincopulated on the nest of a neighbouringing 3 received the visit of a nonmate male with whom they copulated onher own nest. None of the 9 females involved in EPC was paired for morethan five days when EPC occurredand 5 deserted
their mate afterinwith
On each occaanothermale
afterwards.
EPC, pairing
engaging
sion a female participatedin an EPC, her male mate was absent from thecolony. All females engaging in EPC laid eggs at least 12 days after EPC
occurred (mean = 20.3 d 1: 7.5 SD) (Fig. 6). Females were observed flying
to a nest other than their own while the resident male was present in304
in such visits, of which 5 had
23 cases. Eight females participated
EPC.
The
female was repelled ininsuccessful
visiting
engagedpreviously
16 cases by the male alone and by both members of the resident pair in 7
cases.
in successful EPC. Two
to participate
Seven males were observed
ringed males were 5 years old. Five paired focal males were visited by afemale and copulated on his own nest, and two flew to a different nest andwith recently paired females. These two males came from a
copulateddistant part of the colony and were not included in the focal sample,
in EPC
hence their pairing status was unknown. Males who participated
did so between 54 and 15 days before their female mate layed eggs. This ismost surprising because males were more free to spend time away from
Focal males were observed to visit
the nest after the onset of incubation.
others' nests in another 48 cases when resident birds were present: 23 theanotherFig. 6. Upper: the number of EPC performed by female white storks at different times after
pair formation. Lower: the number of EPC performed by female white storks at different
times of her breeding cycle (open dots) and the number of visits by male white storks to nonmate females while they remained alone at her nest, at different times of the breeding cycleof the visited female (black dots). Day 0 is the day of laying of the first egg in the clutch.

305
female alone, 16 the male alone and 9 both members of the resident pair.
Fig. 6 shows that most alone females who were visited by males were notin their MF period. Females attacked and repelled the approachingmale
in all these cases.
of a pair, while present on their nest, were
When both members
anotherthe male attacked the intruder
more frebird,
approached
by
than
the
female(Wilcoxon test, Z=4.13, p<0.001, N=43). Males
quentlymales
and females equally often (Z=1.78,
attackedns) but
intrudingto attack intruding
females over males (Z=2.09,
females preferredp<0.05).
8. Femaledesertions.

Out of 43 paired females at colonies, 9 (21 %) deserted their mate prior toegg laying. Desertion took place 6 days on average after pair formation(range 2-14 days, N=7). Three ringed females were 4, 6, and 6 years old(mean 5.3), while five deserted males were 2.4 years old on average (± 1.144
SD). Females who deserted mates spent significantly
longer amounts oftime alone at the nest during the pair-formation
period (12.3%, ± 2.2 SD,
thanfemaleswho
remained
with
her
first
male mate (6.47%, ± 1.5
N=7)SD, N=35) (Mann-Whitney
test, Z=2.04, p<0.05). In addition, deserting± 0.09 SD) than females
females had lower PC rates (0.39 copulations/h,
who did not desert their mates during the same period (0.49 copulations/test, Z=4.87, p<0.001).
h, ± 0.06 SD) (Mann-Whitney
Discussion
Both female and male white storks breeding at colonies had ample opportunities for engaging in EPC, but they did not. First, EPC in this study
occurred at a frequency much lower (0.4%) than it has been reported for
related colonial species (cattle egret Bubulcus ibis: 29-31 %, FUJIOKA &YAMAGISHI, 1981; MCKILLIGAN, 1990; spoonbill Platalea leucorodia: 19%,
AGUILERA & ALVAREZ, 1989; white ibis Eudocimus albus: 36%, FREDERICK,
1987). Second, EPC were poorly tuned with the female MF period and,
consequently,
any sperm depositedby a nonmate male would have towithfurther
extended over a period ofcompetemany
pair-copulations
several (> 10) days. Studies with domesticatedbirds have revealed that thelast insemination
before fertilization
has priority (BIRKHEAD, 1988). Since
the intensity of sperm competition
should be directly related to the ratioat the time of ovulation,
this means that sperm competiEPC/(PC+EPC)
tion must be necessarily weak or absent in this species. Both males and306
more in extra-pair interactions
females participatedearly in the breeding
cycle, when pairs had just recently formed. This, together with the more
active role played by females in both EPC behaviour and pair formation(see also HAVERSCHMIDT, 1949; COLLIN, 1973; BROWN Bt al., 1982),
strongly suggests that EPC were part of a "mate sampling" strategy (ENS,
strategy (WESTNEAT et al.,1992) rather than of a mixed reproductive1990).
for the lack of EPC in white
We feel unable to advance an explanation
storks. However, our results raise the question of how copulation patterns
Consistent withare to be explained in the absence of sperm competition.
white storks lacked some behavthe apparent lack of sperm competition,iours which have been generally assumed to have evolved as male counto EPC in the context of a Mixed Reproductive
termeasures
Strategy.
Thecoincidenceof PC and EPC or male intrusion pressure with thea)female fertile period (FITCH & SHUGART, 1984; McKINNEY et al., 1984;
BIRKHEAD, 1988; MOCK & FUJIOKA, 1990; WESTNEAT et al., 1990). White
storks lacked tuning of maximum daily EPC and PC rates with the female
MF phase. Many monogamous
species in which EPC are common show a
in
PC
also
near
or at the onset of the female laying period
(and
EPC)
peak
&
which
is a likely adaptation
for minimizing(AGUILERA ALVAREZ, 1989),
the risk of extra-pairfertilizations.
White storks, on the contrary,
drastically reduced PC rates around a week before egg laying, and this effectwas due to both a lower receptivity
by females and a lower rate ofmales.
copulation
attempts byb) The existence of mate guarding (BIRKHEAD, 1979; FORD, 1983; FITCH &SHUGART, 1984; MCKINNEY et al., 1984; MOCK & FUJIOKA, 1990). White
stork males spent less time at the nest during the female MF than pre-MF
has been observed in cattle egrets
period, while the opposite patternand&
YAMAGISHI, 1981)(AGUILERA & ALVAREZ,(FUJIOKA
spoonbills
in
all
these
females1989). Since,
only copulate at the nest, thespecies,
extent of nest guarding
thus
directly reflects effective mate guarding,at the nest during his
females paired to males with a lower attentivenessfemale fertile periods experienced
higher EPC rates (FREDERICK, 1987;
WESTNEAT et al., 1990). Male absence caused females to spend a muchof daytime alone at the nest during their MF period
higher proportion
than before, which is also at variance with the expected pattern underconditionsof sperm competition(e.g. FREDERICK, 1987; AGUILERA &ALVAREZ, 1989; BIRKHEAD & MOLLER, 1992).
of a daily pattern of copulations
which parallels thec) The occurrence
chance of fertilization.
In many birds studied, ovulation
takes place

307
after laying of the preceding egg (CHENG et al.,BIRKHEAD, 1988; CHENG & BURNS, 1988), and any copulation
window"
would maximize
theoccurring
during such a "fertilizationof fertilizing the ova. White storks showed a peak of copulaprobability
tions in late afternoon which was especially marked during the female MF
period. Most (74%) eggs were laid during the morning (0700-1200)(48
window" would be expected on lateeggs, 21 pairs), hence a "fertilization
took place.
morning and not at dusk, when most copulationsof behaviour related to sperm competitiond) The higher prevalence(e.g.
rates or mate guarding) among colonial than among solitarycopulationor populations
nesting
species(BIRKHEAD, 1978; MOLLER, 1985;
BIRKHEAD et al., 1987). Colonial storks did not copulate more than solitaryones, and the lower fraction of time spent at the nest by solitary birds canbe easily explained by the higher risk of nest robbery at colonies.
On the other hand, white stork copulation rates are among the highest
ever recorded for birds: only 4 out of 57 species copulate 160 times per
clutch or more (BIRKHEAD & MOLLER, 1992). In addition,
copulations
extended over a prolonged period (often several weeks) prior to fertilization the eggs. The evolution
rates and extendedof high copulation
in
have
birds
been
copulatory
periods
by invoking selective
explained
relatedtopressures(BIRKHEAD et al., 1987; MOLLER,
sperm competition
BIRKHEAD
of&The
two proposed
1991;
MOLLER, 1992).
advantages
extended copulation
periods are:a) The result of females conceiling ovulation in order to prevent sexual
harassment
males or to obtain benefits provided by theirby non-matemates during the pre-laying
period (THORNHILL, 1984; LUMPKIN, 1981,
1983; BIRKHEAD & LESSELLS, 1988; MOLLER, 1985, 1987b).
b) A way of males for swamping any sperm stored by their female materesulting from previous matings (MCKINNEY et al., 1984; AGUILERA &within a few (< 100) minutes
1987;

ALVAREZ, 1989; MCKILLIGAN, 1990).
The main problem with these hypotheses in the case of the white storkis that they all assume that sperm competition
is an important
selective
force favouring
ovulation
to nonmate
or concealing
sperm swamping
males. However, it is still possible that female storks gained a benefit frommale care during the pre-MF period (mechanism
a above), hence they
were selected to retard ovulation as much as possible (THORNHILL, 1984;
LUMPKIN, 1983). Male white storks neither protected females from sexual
harassment
mates withby other males (LuNIrKIN, 1983) nor provisioned
food (TASKER & MILLS, 1981; MOLLER, 1987a), but gathered and apportioned nest materials. The close association between copulationand nest

308
behaviourby males would mean that females were tradingfor nest materials. A weakeness of this hypothesis is that, by
copulations
in order to obtain a large nest, females would also
ovulation
retardingIn addition, it
andlater clutches were less productive.
delay egg-laying,
and why males
fails to explain why females should not solicit copulations
should attempt to copulate at such high rate. However, the association
between nest building and copulation
could explain why males tended totheirafter collecton
tonest, presumably
copulate immediately
returningasa tactic ofnestmaterial.
This
is
ing
patterncommonly
explained&
assurance
when
the
risk
of
EPC
is
paternity
high (BIRKHEAD MOLLER,
construction1992).
If high copulation
rates in the white stork can neither be explained byconstraints imposed by egg fertilizationor predation pressures, nor as an
to
we
must
consider the possibility that
adaptation
sperm competition,
are
of
a
of
mate
assessment
involved in the
copulations
partprocessof the pair bond (BIRKHEAD et al., 1987;
and maintenanceacquisition
BIRKHEAD & MOLLER, 1992). This hypothesis
assumes that mating is
both
in
terms
of
costly(DALY, 1978; DEWSBURY, 1982)
sperm production
males byhence
femalesand copulating
effort,may choose good-quality
males(DEwsBURY, 1988;
choosing vigorously
courting (i.e. copulating)is
GRAFEN, 1990). That males need a recovery time between copulations
suggested by the fact that intervals between PC by male spoonbills with
EPC by the male mate were longer than those without anan intermediate
EPC (AGUILERA, 1989). Copulations
often occur at times when they have
to
do
with
fertilization
nothing(ELLIS & PowERS, 1982; MGKINNEY et al.,
1984; ROBERTSON, 1986; JAMIESON & CRAIG, 1987; NUECHTERLEIN &STORER, 1989; SODHI, 1991; BIRKHEAD & MOLLER, 1992) but which could
be potentiallyinvolved in mate assessment by females.
Our results on female desertion (also HASS, 1966) support the idea thatfemales preferred to mate with males that copulated frequently and wereless likely to leave them alone at the nest, or beared any trait which
Such a preference
correlatedwith copulation
rate and nest attendance.
could have evolved by two possible mechanisms(KIRKPATRICK & RYAN,
indirectselection
of
for
males
1991): (i)carrying good genes
preferences
for males whofor general vigour, and or (ii) direct selection of preferences
provide resources to offspring.
A prediction
arising from the mechanism of indirect selection for male
is
that
males
more frequently
during the period ofvigourcopulatingassessment (pre-MF) should be heavier and better at obtaining the larger
nests. This prediction was not supported by the available data but sample
sizes were quite small.

309
The possibility that females could employ PC as a cue for male aptitude
for parental care has been repeatedly suggested, but supporting
evidence
is still lacking (FITCH & SHUGART, 1984; MOLLER, 1985; WESTNEAT et al.,1990). We found that PC rates during the female pre-MF period werehighly correlated with rates of chick feeding by males, because males who
spent more time at the nest copulated more frequently. It is likely that theof time a male can remain at the nest without feeding ispercentage
positively related to foraging efficiency (FREDERICK, 1987), which in turn
must be related to the rate of chick provisioning.
That time spent at thenest was dependentconditionof the male, is sugupon the nutritional
the
fact
that
heavier
males
and
males
gested byartificially supplied withfood attended
the nest for longer. Nest and mate guarding
competeswith male feeding activity (BIRKHEAD & MOLLER, 1992). In
temporally
species (e.g. swallows) in which mate guarding lasts for a few days, a large
body mass may allow males to keep on guarding for longer (MOLLER,
1987c), but male reserves may be insufficient when guarding extends overa much longer period. Females could then be able to assess the foraging
the percentage
of dayefficiency of males prior to laying by monitoringtime they spend at the nest and, simultaneously,
imposing them a sensible
cost in the form of frequent
theand, perhaps,
energetic
copulationsofnestmaterials.
Thisstatesthatapportionment
hypothesis
spending
time at the nest and copulating
frequently may be costly forms of mateinvestment. Accordingly,
males should reduce their attentivenessonce thefemale has committed
herself to lay eggs. Male white storks did in fact
when males were provided with
this, and the effect was less important
food. On the other hand, food-supplemented
males copulated less during
the pre-MF
which
seems
not
to
be
in agreementwith thisperiod,hypothesis.
As it stands,

the hypothesis does not state that females can assess thetheir rate of PC. Instead,foraging efficiency of males by monitoringareviewedasofacopulations
partcomplex communicative
system bywhich males advertise their good body condition in spite of guarding
thenest. Monitoring
the duration of male nest guarding is open to cheating
because males could stay at the nest for long periods at the expense of
their own energetic reserves. Unless males spend energy at a high rate
the extent ofduring the period of female assessment, females monitoringmale nest guarding will be assessing the quality of male energy reserves,
instead of their current feeding efficiency. However, the amount of maleenergetic reserves may be decoupled from his current foraging efficiency(e.g. in migrating species, or when adults and nestlings require different
food items). The use of energeticallyfor thecostly signals is required

310of this communicative
reliability
system to remain stable over time
(ZAHAVI, 1977; GRAFEN, 1990). Since the assessment process takes placein the context of mating, copulations
are good candidates
to becomeofaas
costly signalling system. Unlike
incorporated
major components
and thiswhite storks, herons, egrets and ibises are mostly sedentary,
related
to
the
lack
of
a
difference could perhaps be
costly signalling systemin these species.
BIRKHEAD et al. (1987) argued that copulations were unlikely to be usedbecause in most species areby females as a form of male assessment
But as more evidence
ratherthan
whosolicitfemales,males,
copulations.
is accumulated,the opposite turns to be true: females solicit copulations
in 88% of species studied (BIRKHEAD & MOLLER, 1992). However, once
are regarded as courtship signals, they could evolve as a form
copulations
in which the male takes the initiative for copulaof male advertisementtion. Females paired with males able to feed chicks at a high rate may be
selected in turn to increase feeding rates if this improves the number ormales adverquality of fledged chicks (WINKLER, 1987). Consequently,amate
and from
benefit
both
from
their
securing
tisingquality mightInwith thisfemales.
increased rates of chick provisioning
byagreementafemalesalso
showed
rates
of
chick
idea,
by
significant
provisioning
with copulation
correlation
rates, and chick feeding rates by males andfemales were also strongly correlated each other. The "Male Assessment"
hypothesis could also explain why males should reduce PC attempts as
to lay eggs in his
early as they are confident of the female's commitment
BIRKHEAD
etnest. Many monogamousal., 1987) show a
species (e.g.
This
to
in
PC
at
the
onset
of
is problematic
dramatic drop
rates
laying.
the "Sperm Competition"
because daily PC rates decrease
hypothesis
when females still have fertilizable ova, but it makes sense as a reduction
to layin advertisingeffort once females no longer need to be persuaded
the
"Male
Assessof
Inamodifiedmeans
version,costly signals.
eggs byment" hypothesis has also been invoked to explain the high copulation
rates and associated female adaptations
rates, anovula(low conception
and
of
of
felinemammalsoestrus,(EATON, 1978).
synchronyoestrus)tory
tobeusefulatthestudieshavevery
elucidating
Comparative
provedinbirdsmechanisms
thevariation
underlying
copulation patterns among(BIRKHEAD et al., 1987; MOLLER, 1991; BIRKHEAD & MOLLER, 1992). It is
unfortunate,however, that "Male Assessment"
hypotheses fail to provide
a simple variable (like the EPC/(PC+EPC)
ratio in the "Sperm Competiare expected to covary in ation" hypothesis)
with which PC patterns
interests
are likely to vary from
This
is
so
becausefemaleway.
predictable311
species to species and also because the extent to which males advertise byof copulations
to the whole signalling(i.e. the contribution
copulating
also
Two
of
the
"Male Assessment"
system) may
vary.
predictions
are
the
same
as
those
of
the
hypothesis
virtually"Sperm Competition"
hypothesis: (i) higher PC rates among monogamous-polyandrous(having
extensive male parental care) than among polygynous birds (lacking muchcare) (MOLLER, 1991), and (ii) higher PC rates among nonpaternal
see below)
guarders (e.g. raptors, which may also have female-feeding,than among guarders (BIRKHEAD et al., 1987; & MOLLER, 1991).
On the other hand, the first hypothesis
does not predict a direct
between PC rates and the extent of sperm competition
swithinrelationshipthat awaits to be tested. Our resultsmonogamous species, a predictionthat this should be measured
suggest, however,directly (e.g. as theandnotinferredfromanothervariable like theEPC/(PC+EPC)
ratio),
extent of guarding or the degree of breeding sociality. Otherwise, we may
be losing substantial
residual variance in copulation rates which is usefulfor identifying selective pressures (other than sperm competition)
favourrates.
ing high copulation
For example,
in raptors have been extensively
copulation
patterns
as male counteradaptations
to sperm competitionin theexplained
absence of effective mate guarding (BIRKHEAD et al., 1987; BIRKHEAD &LESSELLS, 1988; MOLLER, 1987a, 1991; BIRKHEAD & MOLLER, 1992;
NEGRO et al., in press). In support of this hypothesis,
MOLLER (1987a)
more frequently
found that (i) male goshawks Accipiter gentilis copulated
than usual after returning from a hunt; (ii) males spent a lower fraction of
daytime at the nest site after eggs laying than before; and (iii), acrosswithspecies, copulation
frequency showed a strong positive correlation
the extent of male provisioning
the
and
the
duringpre-laying
egg-laying
however, also make sense under the hypothesis
periods. Such patterns,
that males advertise and females assess male quality by copulation
frestress. MOLLER (1987a)quently during the period of male nutritionalin goshawks. EPC are
actually did not find evidence of sperm competition
characterised
a
low
less
than
usually
by very(often50%) success (FuJIOKA& YAMAGISHI, 1981; FREDERICK, 1987; WESTNEAT, 1987; BIRKHEAD &LESELLS, 1988; NEGRO et al., in press), which lowers the average success of
total copulation
However, more than 99% of all copulationsattempts.
MOLLER
were
successful
analyzed by(see also ROSENFIELD et al., 1991, foranother putative example). In fact, when the extent of mate guarding andis considered,
breeding
density, instead of female provisioning
many
raptorial species are found which do not fit the expected pattern (SIMMONS, 1990).

312
All this claims for the necessity of detailed field studies of the copulation
behaviour of birds as the only way to distinguish among several plausible(and not exclusive) hypotheses. In this context, the search for species witha low degree of sperm competition
will be especially helpful for identiin copulation
additional
factors
for the variation
fying
accounting
patterns.

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Zussammenfassung
Weiβstörche Ciconiaciconiaverpaaren sich ca. 30 Tage vor der Eiablage. In dieser Zeit
kopulierten die Partner häufig (160 Kopulationen/Paar; 04 Kopulationsrate eine Woche
vor der Eiablage drastisch absank. Dem liegen sowohl eine veringerte Anzahl von Kopulationsversuchen seitens des Männchens als auch eine geringere Empfängnisbereitschaft desWeibchens zugrunde. Dieses Verhaltensmuster war unabhängig davon ob die Paare solitär
oder in Kolonien brüteten. Kolonie- und solitärbrütende Männchen verbrachten mehr Zeit