Ethology 82, 230-237 (1989)
0 1989 Paul Parey Scientific Publishers, Berlin and Hamburg
ISSN 0179-1613

Estacion Biologica de Doiiana, Sevilla

Sperm Competition and Copulation Intervalsof the White Spoonbill(Pfatafealeucorodia, Aves, Threskiornithidae)
EDUARDOAGUILERAAGUILERA,
E. 1989: Sperm competition and copulation intervals of the white spoonbill (Platalealeucorodia, Aves, Threskiornithidae). Ethology 82, 230-237.

Abstract
Some aspects of sperm competition were studied in the white spoonbill (Platalea leucorodia)
breeding in Dofiana National Park (SW Spain). Shorter pair copulation intervals occurred during theprelaying period, when females were subjected to a relatively high frequency of extra-pair copulations. Pair copulation intervals with an intermediate extra-pair copulation by the male mate werelonger than those without extra-pair copulation. This result indicates that males need a time ofrecovery between copulations before they can perform another. Extra-pair copulations by the females
did not affect the length of intervals between pair copulations. There were no differences between thelengths of the intervals between an extra-pair copulation by the female and the following pair
copulation for cases in which the male mate detected an intruder male attempting copulation with hismate and those in which the intruder remained undetected. However, the correlations obtained
between copulatory intervals for detected and undetected cases suggest a copulatory response by theirmates, although affected by the required recovery time between copulations by the males. Finally,
since extra-pair copulations mainly occurred while male mates were collecting nest material, theyengaged in this activity shortly after pair copulations, probably to avoid a last-male advantage under
the sperm competition pressure.

Corresponding author: Eduardo AGUILERA,Estacion Biologica de Dofiana. E-41013 Sevilla.

Introduction

When males are uncertain of their paternity, there should be strong selection
favouring adaptations ensuring paternity (PARKER
1970, 1984). Male birds avoid
the effect of cuckoldry by means of two tactics: mate guarding (e.g. BEECHER&BEECHER
1979; BIRKHEAD
1979, 1982) and sperm devaluation (MCKINNEYet al.
U.S. Cupyrighr Clearance Center C o d e Statement:0179-1613/89/8203-0230$02.50/0

Sperm Competition and Copulation Intervals of the White Spoonbill

23 11983, 1984). The evidence presented by BIRKHEAD
et al. (1987) indicates that
copulation frequency of birds increases in relation to the risk of sperm competition. Males ensure in this way a numerical surplus of their own sperm overcompetitors’ sperm and thus increase their probability of fertilizing the eggs(PARKER1984).
Other components of the copulatory behaviour of birds may also have
evolved in a context of sperm competition. Individual male swallows (Hirundorustica) reacted by increasing pair copulation rate when their mates were chasedby other males and, besides, by shortening time intervals between chases andcopulations ( M ~ L L E 1987).
R
Furthermore, it has been observed in some bird
species that pair copulations (forced or unforced) follow immediately after afemale mate has been subjected to an extra-pair copulation (e.g. BARASH1977;
MCKINNEY& STOLEN1982; AFTON1985; BIRKHEAD
et a]. 1988) or following anintrusion by a strange male (references in BIRKHEAD
et al. 1987). However, spermproduction is limited (DEWSBURY1982), and, therefore, males may need a periodof recovery after a copulation before they can perform another. Since an extrapair copulation may occur at any time after a pair copulation, the time interval
between an extra-pair copulation by a female and the following pair copulation
might be a crude measure of the copulatory response by male mates.
Alternative evidence for a paternity ensurance copulatory response by males
might appear from a comparison of the intervals between two consecutive pair
copulations separated by an extra-pair copulation by the female and the intervals
between two pair copulations without an intermediate extra-pair copulation.
Since intervals between pair copulations may be affected by other factors, I firstexamined the effects of nesting cycle, inter-pair differences and extra-pair copulations by male mates on pair-copulation intervals of white spoonbills (Platalea
leucorodia). I then explored evidence for copulatory responses of male mates toextra-pair copulation by their mates.
O n the other hand, since extra-pair copulations mainly occurred while male
mates were collecting nest material (AGUILERA& ALVAREZ
1989), I examined
whether males employed copulatory tactics in connection with this activity toimprove their success under the pressure of sperm competition.
White spoonbills are colonial birds in which males and females share nestbuilding, defence, incubation and nestling feeding (AGUILERA
1988). In anotherpaper, AGUILERA& ALVAREZ(1989) have shown that extra-pair copulation
attempts account for 19 Yo of all copulation attempts, and a minimum of 60 % ofmated males and 75 YO of mated females were involved in extra-pair copulationsat least once. These results suggest a strong selection pressure due to spermcompetition in this population.

Methods
Mating behaviour of white spoonbills was studied at the mixed species heronry of Donana
National Park (SW Spain) during the breeding seasons 1985-1986. The nests of spoonbills wereplaced on cork oaks (Quercus suber) in the border of a brackish marsh (for a general description of the1958). Behavioural observations were done with 10 x 40 binoculars andstudy area see VALVERDE
20-60 telescope from two blinds placed 60 m from the spoonbills’ nests. Each year, 8 to 12 pairs

232

EDLIARDO AGUll E K A

occupying contiguous nests were simultaneously observed from dawn to sunset 3 o r 4 days a weekfrom the onset of breeding until nestlings left the nest. Overall, 4700.9 pair-h from 28 different pairs
were recorded. Individuals were recognized by distinctive features of the light spot o n the upper tip ofthe bill (AGUILEKA& ALVAREZ
1989), and sexes were distinguished by the larger body size of males
and checked by positions during copulation. I recorded the time of each copulation attempt involving
individuals of the study pairs, the identity of the birds and the outcome of attempts. I also registered
the time of each trip to obtain nest material and the identity of the birds.
The breeding cycle of each pair was classified in four periods according to the day when the firstegg was laid (day 0): early prelaying (from the day that the pair occupied the nest site until day - 6 ) ,prelaying (irom day -5 to day -I), laying (from day 0 to day + 6 ) and incubation (from day + 7 until
the day prior to the hatching of the first egg).
Statistics were used following SIEGEI.(1 956). For most statistical analysis I assumed copulations
and copulation intervals to be independent observations.

Results
The nesting cycle significantly affected the time interval between two
consecutive pair copulations (Fig. 1, Kruskal-Wallis one-way analysis of variance, H = 9.16, df = 3, p < 0.05). Shorter copulation intervals occurred during
prelaying. No significant differences of copulation intervals among pairs wereobserved during prelaying, when a sufficient sample size was available(H = 19.7, df = 8, p > 0.05).
Pair copulation intervals separated by an extra-pair copulation by the male
were significantly longer than pair copulation intervals without an intermediate
extra-pair copulation during the prelaying period (pair copulation intervals with-174- h42

99TLw
L 2-Fr-I-B#=E”

3\’Fzg. 1: Nest cycle variation in the meantime interval between pair copulations.
Bars are 1SE. Numbers represent samplesizes

233

Sperm Competition and Copulation Intervals of the White Spoonbill

an intermediate extra-pair copulation by the male: X = 3.95 h, SE = 0.81 h,
n = 7; pair copulation intervals without extra-pair copulation: X = 2.36 h,
SE = 0.22, n = 92; Mann-Whitney U-test, two tailed, U = 136, p = 0.011).
This result indicates that males need a recovery time between two consecutivecopulations.
Intervals between two consecutive pair copulations with an intermediate
extra-pair copulation by the female were shorter (X = 1.79 h, SE = 0.17 h,
n = 9) than those without an extra-pair copulation (%= 2.54 h, SE = 0.22 h,n = 88), although the difference was not significant (U = 433.5, p > 0.05).
Only in two out of 12 cases when the male mate detected an intruder male
attempting copulation with his mate, a pair copulation followed before a 10 min
period elapsed. I analysed differences between all cases in which male mates
detected the presence of an intruder male attempting copulation on their nest(n = 12) with cases in which intruder males were not detected (n = 12). Because

3-G4-'Fig. 2:

Relationship between some copulatory intervals for a) cases when male mate detected theintruder male attempting copulation with his mateand b) cases when the intruder remained undetected.
EPC = extra-pair copulation by the female mate;
P C l = pair copulation before an EPC; and PC2 =pair copulation after an EPC- *E 0t2k 0a)

12

1

3

2

PC1-EPC intervals

453h234

EWARDO AGUILERA

all these extra-pair copulation attempts occurred during the short intervals inwhich females’ mates were collecting nest material and since time differences
between the moment in which an extra-pair copulation attempt occurred and thearrival at the nest by male mates were null when intruders were detected, andshorter than 2 min when they were undetected, I used, for comparative purposes,
the moment in which the extra-pair copulation attempt occurred as “point zero”
in both cases. No differences were found between the mean length of the intervals
between an extra-pair copulation attempt and the next pair copulation for these
two sets (intruder detected: X = 1.02 h, SE = 0.18 h; intruder undetected:
X = 1.00h, SE = 0.33; U = 84, p > 0.05). If males detected an intruder maleand responded by copulating with their mates after a relatively short period, this% 100-$2!!508
E0-% 504!!

8E25l
TIME (min)Fig.3: a) Cumulative reverse distribution of time intervals between two consecutive pair copulations(n = 171); b) distribution of the intervals between pair copulation and nest material trips by males‘n = 203); and c) distribution of the intervals between a pair copulation and the next extra-pair
copulation by the female mate (n = 32)

Sperm Competition and Copulation Intervals of the White Spoonbill

235

period being affected by the length of the interval since the last copulation, then
one should expect a positive correlation between this interval and the interval
between the two pair copulations with this intermediate extra-pair copulation. In
cases where male mates did not detect intruder males, the former interval shouldbe irrelevant and this should not show any correlation with pair copulationintervals. As predicted, the correlation between these two intervals was high andsignificant when a male intruder was detected (r, = 0.81, p < 0.01, Fig. 2) and
low and not significant when an intruder remained undetected (r, = 0.18,

p > 0.05).
The intervals elapsed since and to the previous and the next pair copulation
with respect to an extra-pair copulation were strongly negatively correlated whenmale mates did not detect any intruder male (r, = -0.93, p < 0.01; Fig. 2), while
this correlation was non-significant when an intruder was detected (r, = 0.27,p > 0.05).
The distribution of the intervals between a pair copulation and the next
extra-pair copulation by the female did not depart significantly from the pair
copulation-nest material trip time interval distribution (Fig. 3; KolmogorovSmirnov, two sample test, D = 0.13, n l = 203, n2 = 32, p > 0.05). O n theother hand, male mates collected nest material shortly after a pair copulation in a
proportion greater than expected according to the distribution of time intervals
between pair copulations (Fig. 3; D = 0.58; n l = 171, n2 = 203, p < 0.01).

Discussion
Some male birds copulate with their mates immediately after they have been
subjected to an extra-pair copulation. In this study no significant differences wereobserved among an extra-pair copulation by the female and the following pair
copulation interval for cases when intruders were detected and cases when theywere undetected. These results do not necessarily reflect a lack of copulatory
response by males to extra-pair copulations by their mates but an imposition of
the required recovery time between copulations by males. This is supported byvarious correlations between copulation intervals. An extra-pair copulation by
the female occurring shortly after a pair copulation may not elicit an immediate
copulatory response by her mate because his recovery time between copulations
has not been reached yet. However, if the copulation response is actuallypresented by the male mates, a positive correlation between the interval elapsed
since the last pair copulation until the extra-pair copulation and the interval sincethat copulation and the next pair copulation should be expected. This relationshipwas observed only in cases when male intruders were detected, whereas in thosecases in which intruders remained undetected, the former interval should bemeaningless and thus this correlation should not be expected. For constantinterval lengths, if they are randomly divided in two periods, the longer is one theless is the other and, therefore, a negative correlation between them should beexpected. This is the situation observed in this study for the relationship between
the intervals since the previous and the next pair copulation in relation to an extra-236

EDUARDOAGUILEKA

pair copulation by the female when male intruders were not detected, i.e.
intervals between two consecutive pair copulations were randomly divided;
whereas when the intruders were detected, the correlation was not found,probably due to an “a posteriori” change in the length of the intervals between
pair copulations as a consequence of the copulatory response by male mates.
An important question in connection with the sperm competition is theeffect of the order in time of the inseminations on the fecundation of the eggs.
There are few studies as yet on this topic in birds (see however, COMPTON
et al.
1978; CHENG
et al. 1983; SIMSet al. 1987; BIRKHEAD
et al. 1988) although all ofthem indicate an advantage to the last male copulating, but only when inseminations were separated more than three hours. M 0 L L E R (1988) showed that monogamous bird species with a high intensity of sperm competition copulate frequently, but each ejaculate contains a smaller number of sperm than species withboth low rate of copulations and low intensity of sperm competition. H e suggeststhat this situation has evolved to avoid the last male advantage. The results of thisstudy support this hypothesis. Shorter copulation intervals in spoonbills occurred
during prelaying, when female mates experience the maximum frequency ofextra-pair copulations (AGUILERA& ALVAREZ
1989). By maintaining short intervals between pair copulations, male mates may avoid the priority in egg fecundation by extra-pair copulations of their mates occurring after that critical timeperiod. In this respect, it is also interesting that males collected nest material
shortly after a pair copulation. In doing so, males minimize the intervals between
a pair copulation and the moments when an extra-pair copulation might occur
and thus avoid a possible last male advantage. O n the other hand, the similarity
between the interval distributions of pair copulation-nest material trips and pair
copulation-next extra-pair copulation indicates opportunism by males whenattempting extra-pair copulations.
Acknowledgments
I thank F. ALVAREZ,
J. A. AMAT,A. P. M0LLER and two anonymous referees for comments onan earlier version of the manuscript. The work was supported by ADENA-WWF, Junta de Andalucia
and Consejo Superior de Investigaciones Cientificas.

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VALVERDE,Received: December 12, 1988
Accepted: May 3, 1989 (W. Pjlumrn)