ANIMAL BEHAVIOUR, 1998, 56, 289–299
Article No. ar980788

Copulatory behaviour and paternity in the American kestrel:
the adaptive significance of frequent copulations
M. VILLARROEL*, D. M. BIRD* & U. KUHNLEIN†*Avian Science and Conservation Centre, Macdonald Campus of McGill University†Department of Animal Science, Macdonald Campus of McGill University(Received 20 January 1997; initial acceptance 6 March 1997;
final acceptance 27 October 1997; MS. number: 5458R)

ABSTRACTThe adaptive significance of repeated withinpair copulations is not well understood. We analysed the
copulatory behaviour of 16 pairs of solitary-nesting American kestrels, Falco sparverius, in southernQuebec (Canada), and the achieved reproductive success (paternity) of 21 kestrel families determined by
DNA fingerprinting, in terms of four hypotheses. (1) The paternity assurance hypothesis, which suggeststhat males copulate frequently to avoid being cuckolded, was rejected because there were few extrapair
copulation attempts (<1% of all copulations observed), withinpair copulations were not timed during thefertile period and mate attendance did not increase as the fertile period approached. (2) The immediatematerial benefits hypothesis, which suggests that females trade copulations for food, was refuted because
copulations most often occurred without food transfers, especially outside the fertile period. (3) The
female mate guarding of males hypothesis, which suggests that females distract their mates from othermating opportunities by copulating frequently, was rejected because extrapair copulation attempts were
infrequent, male and female solicitation frequencies were similar and females did not differ in the timing
or frequency of solicitations. (4) The mate assessment hypothesis, which suggests that assessment of matequality is mediated via copulation, most closely predicted the behaviour observed since withinpair
copulations were frequent outside the fertile period and at pair formation, males and females solicited
similar numbers of copulations and pairs did not differ significantly in solicitation or copulation
frequency. In line with this hypothesis we found that only one brood was extrapair, probably the resultof mate replacement.
 1998 The Association for the Study of Animal Behaviour

1992; Keller 1994). Consequently, almost all analyses of
copulatory behaviour in the past two decades describe
frequent withinpair copulations (WPCs) as a paternity
guard (see the paternity assurance hypothesis: Møller
1987; Simmons 1990), for example lions, Panthera leo(Packer & Pusey 1983), sheep, Ovis aries (Hogg 1984),
primates (Møller 1988) and birds (Birkhead & Møller
1992). However, the paternity assurance hypothesis(Simmons 1990), also known as the sperm competition
hypothesis (Birkhead et al. 1987) and the paternity confidence hypothesis (Eens & Pinxten 1995), seems inadequate for at least some frequently copulating species
that have (1) low frequencies of extrapair copulations(EPC; Tortosa & Redondo 1992), (2) copulations before
the fertile period (Negro et al. 1992) and (3) a decreasein frequency of WPCs during the fertile period (Birkhead& Møller 1993). Very few studies consider alternative
hypotheses to the paternity assurance hypothesis andmany lack data on genetic paternity which provides
essential information on reproductive success and has

The majority of vertebrates copulate a few times each
breeding season shortly before fertilization but many
species, from dolphins (Würsig 1989) to birds (Birkhead &Møller 1992), copulate hundreds of times more than isnecessary for fertilization, both during and outside thefertile period. This enormous variation suggests that copulation frequency is under complex selection pressures but
these pressures are poorly understood.
Most detailed investigations of copulatory behaviour
appeared only after it was recognized that postcopulatorycompetition among sperm from different males (spermcompetition) has a significant impact on mating systemevolution (Parker 1970; Smith 1984; Birkhead & Møller
Correspondence and present address: M. Villarroel, Dpto. IngenieríaElectrónica y Comunicaciones, Centro Politécnico Superior 50015
ZARAGOZA Zaragoza, Spain (email: Morris@posta.unizar.es). D. M.
Bird is at the Avian Science and Conservation Centre and U. Kuhnlein
is at the Department of Animal Science, Macdonald Campus of McGill
University, Ste. Anne-de-Bellevue, Quebec H9X 3V9, Canada.
0003–3472/98/080289+11 $30.00/0289

 1998 The Association for the Study of Animal Behaviour

290 ANIMAL BEHAVIOUR, 56, 2

Table 1. Predictions of four hypotheses that explain the adaptive significance of frequent withinpair copulations(WPCs) during the prefertile and fertile periods for birds that do not guard their mates
Hypothesis

Predictions

Paternity assurance(1) WPCs increase in fertile period(2) Mate attendance increases in fertile period(3) Female solicitation increases when paternity confidence is low

Immediate material benefits(1) Females exchange food for WPCs

Female mate guarding of male(1) WPCs occur from pair formation until egg laying(2) Females control copulations via solicitation(3) Females differ in soliciting behaviour

Mate assessment(1) WPCs occur from pair formation until egg laying(2) Both sexes solicit WPCs
(3) Pairs do not differ in solicitation frequency

proven a much more reliable index of cuckoldry than
behavioural observations.
We investigated the adaptive significance of frequent
WPCs in relation to paternity assurance, food-bringing
behaviour and withinpair communication. We tested
four hypotheses (Table 1) that explain why frequent
WPCs occur both outside and during the fertile period inbirds that do not guard their mates: (1) the paternity
assurance hypothesis (Simmons 1990), which suggeststhat males copulate at a high frequency to dilute ejaculates from EPCs; (2) the immediate material benefits
hypothesis (Tasker & Mills 1981; Hunter et al. 1992),
which suggests that females trade copulations (assurancesof paternity) with males for benefits such as food, nest
materials or protection from other males; (3) the female
mate guarding of males hypothesis (Petrie 1992), whichsuggests that females dissuade their males from EPCs by
copulating frequently with them, to reduce the male’s
ejaculate reserves and energy to remate, during, andpre-emptively before, other females intrude on to theterritory; and (4) the mate assessment hypothesis, whichsuggests that individuals may acquire information aboutmate quality via frequent copulation. We suggest thislast hypothesis as a revised version of the male assessment hypothesis proposed by Tortosa & Redondo (1992).
In this way we consider both the male and female
perspective.
We tested these four hypotheses by analysing the
copulatory behaviour of the American kestrel, Falco
sparverius, the most frequently copulating bird (>600
copulations/clutch, Balgooyen 1976; also see Birkhead &Møller 1992). The relevance and predictions of eachhypothesis vary with time and sex since selection pressures may change during the breeding season andbetween males and females. Therefore, we concentrated
our analysis on the timing, success and solicitation of
WPCs from pair formation until incubation. We also
described the frequency of food transfers, EPCs and territorial intrusions and the incidence of extrapair paternity(EPP). We then compared our results with previously
published reports on the copulatory behaviour of otherkestrels and birds of prey.

METHODS

Study Species
The socially monogamous American kestrel is a small
falcon with pronounced sexual size and colour dimorphism (Bird 1988). It is migratory in Canada and defends
a breeding territory of approximately 0.24 km2 (Bowman1985). Both sexes incubate and feed offspring, but hunting during courtship, laying and incubation is done
almost exclusively by the male (Balgooyen 1976). The
American kestrel is thought to practise a mixed reproductive strategy (sensu Trivers 1972). Extrapair copulations(Childs & Mossman 1952; Cade 1955; Willoughby &Cade 1964; Balgooyen 1976; Bird 1988), territorial intrusions (Balgooyen 1976), mate switching (Bortolotti & Iko
1992), polygynous trios (Towers 1990; De Lucca 1993)
and helpers at the nest (Wegner 1975) have all been
observed, although these behaviours may not be widespread (Bird 1988). Female kestrels can also store sperm insperm storage tubules (Bird & Buckland 1976; Bakst &Bird 1987) which allows different males to compete forpaternity of the four or five eggs that normally make up a
clutch (Bird 1988).

Study Areas
We observed wild American kestrels nesting in nestboxes during 1992–1993 in southwestern Quebec(Canada; 4525 N, 7505 W). All boxes were erected ondead hardwood trees in hedgerows bordering fallow fields
or telephone poles along secondary roads. The distance
between observed nestboxes ranged from 500 to 1500 m.
Kestrels did not appear to be philopatric (<2% bandreturns in 1993).
American kestrels in our area have been extensively
studied in the past decade. They show little or no interyear pair or site fidelity and a high incidence of interyear
divorce and death (Bowman et al. 1987). Lifjeld &Robertson (1992) suggested that temporary mate removal
studies are important in order to test the paternity assurance hypothesis. Bowman & Bird (1987) established theVILLARROEL ET AL.: KESTREL COPULATION PATTERNS 291

existence of a floating population of unmated birds in ourstudy area and performed a mate replacement study on
16 pairs during incubation. They found that 50% of males
were replaced after an average of 36 h and that no
replacement pair successfully reared any young.

Focal Observations
Beginning in mid-March, we visited nestboxes every
other day until the kestrels arrived (usually in late March),which allowed us to observe early courtship. We chose
seven pairs in 1992 and nine in 1993 for systematicrecording of behaviour from pair arrival until the end oflaying, while we visited the remaining occupied nestboxes once a week. We selected focal pairs according toarrival time and ease of observation. In 1992, we chose
three pairs that arrived early on the breeding territory(late March) and four pairs that arrived with mostmigrants (April). In 1993, we chose two early pairs, four
pairs that arrived with the majority and three late pairs.
In 1992, the average arrival date of focal pairs was 7 April,in 1993, 9 April (no significant difference between years,
Wilcoxon two-sample test: Z=0.25, N1 =7, N2 =9, P=0.80).
Average laying dates were 30 April in 1992 and 29 April in
1993 (no significant difference between years, Wilcoxon
two-sample test: Z=0.23, N1 =7, N2 =9, P=0.80).
A hidden observer observed focal individuals using
binoculars and a 20–60 telescope, positioned 100–
150 m from the nest. Each pair was observed once
every 2 days during a 1-h (1992) or 2-h (1993) period.
These observation periods were evenly distributed
throughout the daylight hours following a rotationalschedule from dawn to dusk. In 1992 each observation
bout lasted a meanSD of 8634 min (N=59) and in
1993 10746 min (N=196; for description of pairidentification see Blood sampling below).

Analysis of Copulatory Behaviour
For each copulation observed we noted solicitation,
success and individuals involved. Copulations involved
few preliminaries except solicitation (also see Balgooyen1976). We considered a copulation solicited when, before
the male mounted the female, the female moved towards
him and lifted her tail to expose her cloaca (see Roest
1957). Copulation was classified as male initiated if themale moved towards the female and mounted her with
no apparent solicitation. Copulation was consideredsuccessful when cloacal contact was believed to haveoccurred (male lowered tail to join cloacas). We timed
copulations to the nearest 0.1 s using a chronometer. We
observed only two aerial displays (for description see
Village 1990) and they were not analysed.
Copulatory behaviour was analysed relative to thefemale’s fertile period. We synchronized the observation
dates of each pair about day 0, the day the first egg waslaid. The copulation period of each pair was divided into
two periods: prefertile and fertile. The prefertile period
was from the first observation of the pair (usually the day
the pair arrived on the territory) until the onset of thefertile period (day 12, Bird & Buckland 1976). The
fertile period was from day 12 until the end of egg
laying (day +8). The two periods together comprised
approximately 34 days. To estimate day 0, we checked thenest when it appeared the female was brooding and,
thereafter, every 4–5 days. For each egg observed, we
counted back 2 days (since eggs are typically laid every
48 h in the American kestrel, Bird 1988) to estimate the
day the first egg was laid. Finally, we estimated thenumber of copulations per pair in the breeding season
using the following equation: (copulations observed÷
hours observed)days observedhours of daylight.

Associated Behaviours
Several hypotheses that explain repeated copulations inbirds predict that food transfers, intrusions and mateattendance are associated with copulation (Table 1). Foodis transferred (from male to female) from pair formation
until the end of incubation. In our area, meadow voles,
Microtus pennsylvanicus, were the main food transferred(62% of all transfers). Intrusions were defined as the entry
of nonpair kestrels into the breeding territory of thenesting pair (an area of ca. 0.240.04 km2 (XSE) in our
kestrel population; Bowman 1985). We recorded mateattendance as the time the observer estimated that the
male and female of a pair could see one another and/or
the time both individuals were within 100 m of eachanother. In addition, for each pair we recorded arrival
date, laying date, breeding success (number of nestlings)
and incidence of EPFs by DNA fingerprinting.

Statistical Analysis of Behaviour
We analysed data on bird behaviour and pair characteristics using SAS (SAS Institute 1987). Although variancein most behaviours was homogeneous, most data were
not normally distributed (except where noted). Frequency values of behaviour were usually ranked into
groups and ranges of values were low. For all thesereasons we used nonparametric statistics. For correlations
we used Kendall’s tau-b correlation coefficients, where
Z=tau-b/(asymptotic standard error) was a test of significance of tau in terms of a normal distribution (Freeman
1987).

Blood Sampling
From March to July in 1992 and 1993 we took blood
samples from 65 adults and 122 nestlings and we used 21
whole families, 21 putative fathers, 21 putative mothers
and 89 nestlings (X=4.3 nestlings per pair, range 2–5) inthe DNA analysis. Five of the 21 families were focal pairs
we had observed closely. The other 16 nests were each
visited at least five times during the breeding season. We
attempted to catch the adults as early in the breeding
season and as close to the nestbox as possible to colourband individuals and confirm that they occupied the nest
where caught. However, individuals captured within thefirst 2 weeks of arrival often abandoned their nest sites.

292 ANIMAL BEHAVIOUR, 56, 2

DNA Fingerprinting
DNA fingerprinting methodology was as described in
Negro et al. (1996). Briefly, we took 0.3 ml of blood fromthe jugular vein of each captured American kestrel using
an EDTA-coated 1 cc syringe and a 28 gauge needle. DNA
was later extracted from blood cells using a protocol
modified from Jeffreys & Morton (1987). Aliquots of 5 ìgof DNA were digested with restriction enzyme Hinf I(Wolfes et al. 1991) and samples were run (15 per gel) on
0.7% agarose gels at 30 V for 36 h in a 1TPE buffer(pH=8.0). Gel hybridizations were carried out according
to Zishler et al. (1989) using 32P-labelled simple sequenceoligonucleotide probe (GGAT)4. Autoradiography was atroom temperature without intensifying screens for an
average of 3–4 days of exposure. Banding patterns were
only compared between individuals on the same gel andthe lanes of nestlings were flanked by those of theirputative mother and father. The position of the mostintensive bands were scored for each lane (band-sharing
analysis followed Negro et al. 1996). We assumed thatbands assorted independently since a previous studyof six families of captive birds originating from ourwild population of kestrels found no sex-linked bands(Cunningham 1995).
RESULTS

Copulatory Behaviour
Timing
Kestrel pairs copulated frequently during the prefertileand fertile periods (Table 2). The highest frequency was atpair formation (peaking on day 18; Fig. 1) after which
WPC frequency decreased to zero by day +8.92.68(XSD; the end of egg laying). Of 385 copulations
observed, 45.1% occurred before the fertile period began(before day 12). Copulation frequency decreased as
the breeding season progressed and was significantly
lower during the fertile period than the prefertile period(Wilcoxon signed-ranks test: Z=4.3, N=16 pairs,
P<0.001). Thus, copulation frequency was highest when
the female was not fertile.

Success and duration of copulations
The majority (81%) of all copulations observed wereconsidered successful, 13% unsuccessful and 6% were not

Table 2. Average copulation frequencies (per h) of 16 American
kestrel pairs observed in Quebec (Canada) in 1992 and 1993

Pair

Hours
observed

Prefertile
period(cop/h)Fertileperiod(cop/h)Copulations
observed

1992
MA
92F
W25
DV20
92L
92R
W14

25
17
16
13
12
19
12

1.36
1.00
0.50
0.83
0.38
1.40
1.00

0.43
0.63
1.00
0.50
0.25
0.86
0.20

21
13
14
7
4
17
3

1993
C2
DV20
93I
W9
92L
C8
D1
92N
93D

18
40
36
41
31
53
45
29
40

0.00
3.85
3.23
0.00
0.00
1.99
0.96
0.00
1.18

0.89
0.71
0.74
0.38
0.61
0.88
0.50
0.77
0.78

16
49
52
18
19
56
34
26
36

3

Copulations per hSome focal individuals (five of 32) were trapped andcolour-banded before observations began but we left mostindividuals (20 of 32) unbanded. They were identified
by plumage characteristics (highly variable in American
kestrels, Parkes 1955) and behavioural habits during eachobservation bout. Although quite reliable, this approachdiminished the probability of observing mate switching.
To limit the probability of capturing ‘floaters’ we
attempted to capture adults at the nest. Of the 21 families
analysed, 18 females (86%) and 13 males (62%) werecaught inside the nestbox during the incubation period.

2

Fertile period

1

8
3
6
10 12 15 16 13 13
4005
10 15 20
–30 –25 –20 –15 –10 –5
Day in breeding season relative to egg laying (day 0)
Figure 1. Average copulation rates of wild American kestrels in
Quebec (Canada) during the prefertile and fertile periods. Numbers
above the X-axis are the numbers of pairs observed during each timeinterval. Error bars are the standard error of the mean, 0=date firstegg in clutch was laid, and the fertile period, day −12 to day +8,
includes maximum sperm storage duration of 12 days before thefirst egg is laid (see text).

classified. Only one copulation (0.3% of all copulations
observed) was an EPC. The duration of copulations
increased significantly during the fertile period (paired t
test: t109 =2.84, N=9 nests, P<0.05; Fig. 2, Table 3). The
frequency of WPCs was negatively correlated with theduration of copulation (Kendall’s ô= 0.123, N=111,
P<0.05) and the frequency of unsuccessful WPCs
washigher in the prefertile period (Wilcoxon signed-ranks
test: Z=2.0, N=9 pairs, P<0.05).

VILLARROEL ET AL.: KESTREL COPULATION PATTERNS 293

males, P<0.001) although the frequency did not differ
between males (Kruskal–Wallis test: ÷28 =9.94, NS).
Of the copulations that failed (N=39), 64% were initiated by males, 30% by females and 6% were unclassified.
There was no significant difference in the rate of unsuccessful copulations when solicited by females or initiatedby males (Wilcoxon signed-ranks test: Z=0.216, N=9
pairs, NS). Males were occasionally observed to reject
female solicitations (N=11), either by flying away orremaining motionless. Finally, we noticed that females
could end copulations by turning their head back towards the mounted male and sometimes biting (<4% of
copulations).

Duration of copulations (s)

10

8

6

4

2
Fertile period
0–30 –25 –20 –15 –10 –5
05
10 15 20
Day in breeding season relative to egg laying (day 0)

Figure 2. Average duration of copulations among wild American
kestrels during the prefertile and fertile periods. Error bars are thestandard error of the mean and 0=date first egg in clutch was laid.
Table 3. Average frequencies of analysed behaviours (per h±SD,
except duration) associated with withinpair copulation (WPC) frequency in the American kestrel in Canada
Behaviour

Prefertile
periodFertileperiodUnsuccessful WPCs
Duration of WPCs (s)Solicitation by female
Initiation by male
Mate attendance

0.23±0.375±2.1
1.05±1.23
0.92±0.65
0.56±0.37

0.10±0.277±3
0.42±0.68
0.27±0.40
0.47±0.32

Associated Behaviour
Food transfers
We observed 68 food transfers (N=10 pairs, XSD=
7.41.8 food transfers each). The frequency of foodtransfers per h was not significantly correlated withcopulation frequency (Kendall’s ô=0.07, N=255, NS).
Nests where food transfers were observed did not differ
significantly in their copulatory frequency compared tonests where no food transfers were seen (Wilcoxon
signed-ranks test: Z= 1.20, N=16 pairs, NS).

Territorial intrusions

Extrapair copulations
We observed only one EPC which took place on day
11 at a nest site where the nearest nest was 500 m away.
The intruding female, a recent arrival in the study area,
approached the resident male at his perch by his nestbox
and attempted to enter the nestbox. The resident female,perched close by, attacked the intruder and then went
into the nestbox. Then the intruder perched on top of thenestbox and was mounted by the resident male for 3 s.
The resident female exited the box and drove the intruder
away. The resident pair then copulated. They copulated
again 20 min later, at which time the same intruder
female returned and attacked the pair, stopping the
copulation. The resident female chased the intruder
female again and then entered her nestbox.

Solicitation
Males and females initiated copulations at similar frequencies. Of all copulations observed, 50% were solicitedby the female, 40% by the male and 10% were notcategorized. Solicitation by the female did not differ
significantly between the prefertile and fertile periods(Wilcoxon signed-ranks test: Z=1.76, N=9 females, NS)
nor between females (Kruskal–Wallis test: ÷28 =10.9, NS;
Table 3). Initiations by the male were higher in theprefertile period (Wilcoxon signed-ranks test: Z=4.5, N=9

We observed 30 intrusions, 87% female and only 13%
male. Intrusions were brief (XSD=3.52.64 min,N=30). Male and female intrusions occurred throughout
the breeding season although not for all pairs. However,pairs that suffered intrusions did not copulate more thanthose where no intrusions were observed (Wilcoxon
signed-ranks test: female intrusions: Z= 1.54, N=16
nests, NS; male intrusions: Z=1.5, N=16 nests, NS). The
occurrence of female intrusions was not significantly
correlated with female solicitations (Kendall’s ô=0.04,
N=111, NS) nor were male intrusions correlated withmale initiations (Kendall’s ô=0.07, N=111, NS). At two
nests we observed a ‘floater’ female staying within 500 mof the pair for up to a week and repeatedly intruding tosolicit copulations from the paired male.
Female intruders always approached the resident maleand often called to the male and assumed a soliciting
stance. When present, resident females attacked andchased the intruding female off the territory. The
majority of female intrusions (53%) were followed by a
WPC either during or after the intrusion (X=7.25 minafter the intruder’s departure). Of 16 copulations that
followed female intrusions, 31.3% were solicited by thefemale, 18.7% were initiated by the male and 50% were
not categorized.
Of the four male intrusions observed, two were at one
nest on different days (19 and day +3) and two atdifferent nests on days 19 and 2. Male intrusions
lasted, on averageSD, 2.752.06 min (N=4). In allcases, the resident male was on the territory. Once weobserved an intruding male approach a resident female(day +3), after which the female immediately joined hermate at their nestbox where they copulated.

Mate attendanceMate attendance (for definition see Methods) averaged
49.5% and did not vary significantly between the prefertile and fertile periods (Wilcoxon signed-ranks test:
Z=1.68, N=16 pairs, NS; Table 3). Pairs differed significantly in their mate attendance (Kruskal–Wallis test:
÷215 =47.7, P<0.001) and males that spent more time with
their mates copulated more frequently (Kendall’s ô=0.36,
N=255, P<0.001). Mate attendance was not significantly lower in the pairs that incurred male intrusions(Wilcoxon signed-ranks test: Z=0.7, N=16 pairs, NS),
indicating that male presence did not seem to have aneffect on intrusions by extrapair males.

Interpair Comparisons
Copulation
To calculate the average copulation rate per season perpair and to take into account variances in copulation
frequency throughout the breeding season, we averaged
copulation frequencies across the prefertile (arrival to day13), prelaying (day 12 to day 1) and laying periods(day 0 to day +10) for all pairs. For the prefertile period,
we calculated an averageSD of 230145 copulations(N=12, range 43–440), for the prelaying period 15165
copulations (N=16, range 45–275) and for the laying
period, 7325 copulations (N=12, range 26–109). Averaging these frequencies we obtained 45478 copulations
per pair per clutch (N=16) or approximately 13.6 copulations per day. See Table 2 for differences between pairs in
copulatory behaviour. Pairs did not differ significantlyin their copulatory frequency (Kruskal–Wallis test:
÷215 =24.1, NS).

Days from arrival until first egg was laid

294 ANIMAL BEHAVIOUR, 56, 2

35
30
25
20
15
10
5

0
5
March

10

15

20
25
April
Date of pair arrival

30

35
40
May

Figure 3. Dates of arrival and laying for 16 pairs of solitary-nesting
American kestrels in 1992 ( ) and 1993 ().

Arrival and laying dates
Copulation frequency was not significantly correlatedwith arrival or laying date (Kendall’s ô= 0.05, N=255,
NS and ô= 0.07, N=255, NS, respectively). Thus, pairs
did not differ significantly in copulation frequency eventhough the difference in arrival and laying dates between
pairs was sometimes 3–4 weeks (see Fig. 3).

Breeding success
Breeding success was either zero, four or five nestlings
per nest. Copulation frequency of pairs did not vary significantly with brood size (Kruskal–Wallis test: ÷22 =4.1, NS).

Figure 4. DNA fingerprints of one American kestrel family with no
extrapair paternity. Each vertical lane corresponds to one individual.
F=female, M=male, N=nestling.

Extrapair Fertilizations

offspring from their putative mother. We found two
broods (10% of families, 11.2% of nestlings) in which
none of the nestlings was related to the putative father.
All neighbouring males were checked by DNA fingerprinting as possible fathers but none was implicated.

We obtained the genetic fingerprints of 21 families (42parents and 89 offspring) (Fig. 4). The oligonucleotide(GGAT)4 probe revealed a meanSD of 12.22.99 bands(N=131) and few unique bands (Fig. 5). A comparison of
the bands of eight unrelated individuals revealed a low
background band-sharing coefficient (0.1310.114,
range 0–0.33). Thus, the probability of making a false
claim of band sharing was 0.1315.80 =7.5810 6 following Bruford et al. (1994). The sexes did not differ substantially in the number of bands scored (males: 5.482.04,
N=21; females: 5.671.49, N=21). All nestlings wereDISCUSSION

Paternity Assurance
American kestrels copulate more frequently than isneeded to fertilize a clutch. Although WPC frequency is

VILLARROEL ET AL.: KESTREL COPULATION PATTERNS 295

1

Band-sharing coefficient

0.8
0.6
0.4
0.2
0

–0.2
–0.4

0

1

2

3
4
5
6
7
Number of unique bands

8

9

10

Figure 5. The proportion of shared bands (band-sharing coefficient)versus the number of unique bands found in American kestrel
nestlings but not in either parent.

probably the highest of all birds, EPCs were rare (<1%)
compared with most birds (5.9%, Birkhead & Møller
1992) which suggests a low intensity of sperm competition. Approximately half of all copulations observed wereoutside the fertile period which also suggests a secondaryrole for copulations besides that of paternity assurance.
An important assumption of the paternity assurance
hypothesis is that ‘extra-pair copulations and thus spermcompetition are sufficiently frequent to cause a highcopulation rate’ (Møller 1987). Our data do not appear to
support this hypothesis since we found EPC attempts
were very low and presumably not frequent enough tolead to a high WPC frequency.
From our results it appears that the low number of EPFs
observed is the result of a lack of EPCs and not of a
sophisticated anticuckoldry defence system, as concluded
by Warkentin et al. (1994) for merlins, Falco columbarius.
Our results contradict previous studies on other raptors(Robertson 1986; Møller 1987; Birkhead & Lessells 1988;
Simmons 1990; Sodhi 1991; Holthuijzen 1992; Koga &Shiraishi 1994) which conclude that sperm competitionis high and is the main cause of a high copulation
frequency.
Despite our findings, we cannot completely reject theidea that frequent copulations during the fertile period
may act to dilute sperm from the few males that gain
EPCs. Although EPFs occur infrequently in kestrels (alsosee Negro et al. 1996), these falcons maintain a very highWPC frequency throughout the laying period comparedwith other birds. This behaviour may have evolved toenhance the probability of fertilization. However, EPC
attempts should occur if high copulation rates are to be
explained by sperm competition (Tortosa & Redondo1992).
Even if we assume that our rate of EPCs is a low
estimate, that is, we missed observing some EPCs or more
intensive observations would have revealed a higher incidence, three major predictions of the paternity assurance
hypothesis were not supported. First, female solicitation

did not increase as the fertile period approached nor did
females solicit more copulations in pairs that incurred
intrusions. Second, although intrusions occurred, malekestrels did not protect their parental investment more byincreasing mate attendance during the fertile period.
In addition, males initiated more copulations in theprefertile period. Third, even considering the maximum
sperm storage interval of 12 days (Bird & Buckland 1976),
withinpair copulations were common outside the fertile
period and decreased in frequency during the fertile
period. We did not test the insemination window
hypothesis (a secondary hypothesis of the paternity
assurance hypothesis; Birkhead & Møller 1992), thatmales preferentially copulate with females immediately
after each egg is laid, because it is confusing and has
recently been criticized by its former proponents(Birkhead et al. 1996).
Since we knew the maximum length of sperm storageof female kestrels we could distinguish between copulations that could have a role in fertilization and those that
could not (Bird & Buckland 1976). We were thus in agood position to test the paternity assurance hypothesis.
Previous studies of raptor copulatory behaviour did not
make this important distinction. Many species of raptors
show unexplained prolonged copulatory periods with an
early peak of copulations probably outside the fertile
period: lesser kestrel, Falco naumanni, 65 days before
laying (Negro et al. 1992), European kestrel, Falco tinnunculus 20 (Meijer & Schwabl 1989), goshawk, Accipitergentilis, 30–40 (Møller 1987), osprey, Pandion haliaetus,
16–20 (Birkhead & Lessells 1988), prairie falcon, Falco
mexicanus, 27 (Holthuijzen 1992). The paternity assurance hypothesis may not fully explain the copulatory
behaviour of these raptors either.

Extrapair Paternity in Kestrels
The results of our paternity study are similar tofour recent reports of low paternity in Eleonora’s falcon
F. eleonorae (0%, Swatschek et al. 1993) the merlin (0%,Warkentin et al. 1994), the colonial lesser kestrel (3.4%,
Negro et al. 1996) and the European kestrel (5%,Korpimäki et al. 1996). However, our percentage of EPFs is
not directly comparable to other birds since the extrapair
male achieved exclusive paternity. We found no term
to describe a completely cuckolded nest and suggest‘extramale take-over’ as opposed to EPF. The one weobserved may be due to a mate replacement that we did
not observe or we might have caught the wrong male andnot identified him correctly. Depending on the time
between pair formation and egg laying, females could
conceivably arrive on the breeding territory alreadyinseminated (Quay 1989), although this has not yet been
documented in raptors. We suspect a mate replacement
occurred since, in most cases of EPF in birds, extrapair
young represent either a minority or majority of thebrood and hardly ever all the young (also see Birkhead
1996). Completely cuckolded nests have also been
observed in the European kestrel (Korpimäki et al. 1996)
and the lesser kestrel (Negro et al. 1996) as well asother birds (Westneat 1988; Oring et al. 1992; Pinxten

296 ANIMAL BEHAVIOUR, 56, 2

et al. 1993) and are most probably due to rapid matereplacement. More inseminations involve greater sperm
precedence and assurance of paternity (Hatch 1987;
Birkhead & Møller 1992). Although it is currently
unknown if one or several EPCs can fertilize all the eggs ina clutch, physiological evidence suggests not (Birkhead
1996) and for kestrels it is difficult to explain how
one EPC may take precedence over more than 10 WPC
per day.

Immediate Material Benefits
The immediate material benefits hypothesis (Tasker &Mills 1981) suggests that females trade copulations (assurances of paternity) with males for benefits such as food,nest materials or protection from other males. Most
copulations we observed occurred without food transfers.
Several authors have suggested that food transfers are
related to copulation in raptors (for review see Carlier &Gallo 1995), but other studies have found no statisticallysignificant relationship between the two (Birkhead &Lessells 1988; Simmons 1990; Negro et al. 1992; Koga &Shiraishi 1994; Green & Krebs 1995). Since many falconiforms differ in the synchrony of food transfers andcopulations this discrepancy is understandable. Foodtransfers may sometimes be associated with copulationsand ‘feeding of females by males appears to be part ofthe system of mutual sexual arousal’ (Kostina & Panov1979). Females, however, did not solicit more after foodtransfers, suggesting that they do not trade food for
copulations.

Female Mate Guarding of Males
The female mate guarding of males hypothesis (Petrie
1992) suggests that females dissuade their males from
EPCs by copulating frequently with them. Unlike thepaternity assurance hypothesis, the female mate guardingof males hypothesis suggests that females with lowquality males will solicit fewer WPCs. The first two
predictions of this hypothesis were upheld, namely,
females solicited copulations from pair bonding until egg
laying and solicited more copulations than males when
there was a risk that their male could mate with otherfemales (i.e. during female intrusions). In general, however, females did not solicit more copulations than males.
It appears that the copulatory act is initiated by both
sexes and not controlled exclusively by the soliciting
female. In addition, all pairs copulated at similar frequencies and all females solicited at a similar rate. Thus,
the third prediction, that females with high-quality males
will copulate and solicit more copulations than otherfemales, was not upheld, although some paired males
may be more attractive than others (i.e. some males
incurred more female intrusions and participated in more
EPCs).
We did not test a fourth hypothesis of the female mateguarding of males hypothesis, that ‘within-pair copulation frequency will be negatively correlated with the
male’s investment in extra-pair copulations or polygyny’(Whittingham et al. 1994), since it is tautological (Eenset al. 1995; Whittingham et al. 1995). For example,
although males do not appear to need guarding in our
population because they hardly ever partake in EPCs this
could mean that (1) females guard their males well andtherefore suffer low mate loss, or (2) females need not
solicit so many copulations to guard their males because
males do not need guarding.
Instead, one important result allows us to reject thishypothesis definitively. Namely, females did not solicit
most or all copulations, as seen in other birds where thishypothesis may apply (Eens & Pinxten 1995). In our
population the female tactic of soliciting copulations toguard their mates may not always work. Even if females
would like to guard males and are following a best-of-abad-job strategy (Eens et al. 1995), female–female
aggression seems a less expensive method to combat
female–female competition for mates (Slagsvold & Lifjeld
1994; Whittingham et al. 1995). This is what we
observed. The majority of female intruders were physically expelled from the territory by the resident female.
Females were often battling for possession of the male or
territory (also observed by Bortolotti & Iko 1992). Thissuggests that extrapair, female-solicited copulations areprevented by female–female aggression, as seen in otherbirds (Wittenberger & Tilson 1980).
Although we did not quantify the relative roles of males
and females in reproduction, it appeared that primarymale investment was high enough for females to fightover males. In addition, females were not receptive to
EPCs, effectively increasing the male’s net gain of behaving parentally and decreasing the possibility of the maledeserting (for discussion of these points see Westneat
et al. 1990 and Fitch & Shugart 1984). This makes sense
since the male provides essential food resources during
laying and incubation (Bird 1988) and the female cannot
rear nestlings alone in the wild (Village 1990; personalobservation). Our observations demonstrate that females
fight to obtain this limiting resource. Consequently, malechoice may be more important in kestrels at pair bonding
than female choice, which has proven difficult to quantify in kestrels (Duncan & Bird 1989; Bortolotti & Iko
1992; Palokangas et al. 1992).

Mate Assessment
Finally, the mate assessment hypothesis states that
individuals may acquire information about mate quality
via copulation. There have been few analyses of copulations as courtship communication in birds but muchresearch has been done on mammals (e.g. Bastock 1967)
where intromission may be ‘courtship communication in
the tactile modality’ (Dewsbury 1988). Many authors
have proposed that copulation may be used to assess thequality of an individual (Fitch & Shugart 1984; Westneat
et al. 1990; Hunter et al. 1992; Tortosa & Redondo 1992).
Specifically, it has often been suggested that males
honestly advertise their aptitude for parental care or
fitness by performing energetically costly copulations (seethe male assessment hypothesis, Tortosa & Redondo1992). In birds where parental care appears equal for both

VILLARROEL ET AL.: KESTREL COPULATION PATTERNS 297

sexes (as in raptors, Newton 1979), male choice may bejust as important as female choice (Gladstone 1979;
Andersson 1994). Thus, it is in the interests of both males
and females to choose the fittest mate. Therefore we
amplified the male assessment hypothesis to include
assessment of females by males. The male assessment
hypothesis suggests that males honestly advertise theirbody condition by performing energetically costly
copulations and females choose males according toquality. Although this hypothesis, like the paternity
assurance hypothesis, suggests that withinpair copulations should be higher in species with extensive malecare, it predicts that they should peak at the time of pairformation and decrease ‘as early as the male is confidentof the female’s commitment to lay eggs in his nest’(Tortosa & Redondo 1992).
Four predictions of the mate assessment hypothesis
were upheld, namely; withinpair copulations were frequent both outside and within the fertile period, andwere initiated equally by both sexes, pairs did not differ
significantly in solicitation or copulation frequency,
and individuals (intruders) moved away from territories
where potential mates did not attend to theirsolicitations.
Of the four hypotheses we considered, the mateassessment hypothesis best explains our observations. In
addition, this hypothesis helps us to evaluate the increasein copulation duration between the prefertile and fertile
periods.
According to the paternity assurance hypothesis, theimmediate material benefits hypothesis and the female
mate guarding of males hypothesis, copulations areequally potent during and outside the fertile period since
the male is unaware of the female’s fertility status. However, copulations outside and during the fertile period
seem to be different. Prefertile period copulations may becalled ‘courtship copulations’ since they are not involvedin fertilization. We suggest that early copulations inkestrels may be used as courtship communication of matequality. As the fertile period approaches, the character ofthe copulatory act changes to adapt to its primary role asa conduit for fertilization without necessarily losing its
secondary role of mate assessment, since an individual’s
quality may change over time (Hunter et al. 1992). Thischange in the character of copulation is displayed in theAmerican kestrel by copulations becoming longer as thefertile period approaches, which is also seen in otherraptors, for example, bald eagle, Haliaeetus leucocephalus(Laszlo & Retfalvi 1965), gyrfalcon, Falco rusticolus (Wrege& Cade 1977), peregrine falcon, Falco peregrinus (Ratcliffe1980), and may be a generalized form of courtship communication, similar to that seen in mammals (Dewsbury1988). In addition, we observed that female kestrels could
end copulations (control their duration). This has been
observed previously in kestrels (Bishop 1925), peregrine
falcons (Gallo et al. 1991) and black kites, Milrus migrans(Koga & Shiraishi 1994). We suggest that the female
allows copulations to last longer just as the fertile period
approaches.
As with previous studies, we assumed that all WPCs andEPCs, in or outside the fertile period, involved the trans-

fer of sperm. We do not know if early copulations involve
sperm transfer but, in the American kestrel, sperm is
produced 72 days before laying (although early sperm
appears more abnormal in shape, Bird & Lagüe 1977). The
mate assessment hypothesis does not make assumptions
about the cost of WPCs. Theoretically, the cost of one
copulation should decrease as the number of copulations
increases (Parker 1984). Although no physiologicalstudies have been made, the cost of one copulation/
insemination in frequently copulating birds may be verysmall.
How information is transmitted between mates by
copulating is yet to be revealed. In mammals, multiple
copulations, with or without ejaculation, affect sperm
numbers, facilitate sperm transport, mediate female
receptivity and produce neuroendocrine reflexes(Dewsbury 1988). This may occur in birds as well. For
example, the copulation patterns in our population arequite similar to changes in androgen levels in captive
American kestrels that originated from our study area
(Rehder et al. 1988).

Conclusions
We conclude that sperm competition is low in theAmerican kestrel and that copulatory behaviour is not
significantly related to food transfers or female mateguarding of males. Intrasexual competition among males
for fertilizations seems low and both sexes avoid extrapair
interactions. We suggest that copulations are frequentbecause they may serve two distinct and important purposes: (1) fertilization (during the fertile period); and (2)mate assessment during the prefertile and fertile periods.
We suggest that further research on copulatory behaviourin raptors should consider the reproductive physiology ofcourtship communication via copulation.
Acknowledgments
We thank J. J. Negro, J. Fernandez Layna and P. Molina
for helping with the field observations, Mr G. Begin and
I. Giroux and the Dorion division of Hydro-Quebec
servicemen for permission and upkeep of nestboxes on
telephone poles, I. Ritchie, M. Adam, G. Barret, A. ReuterCortes and M. Gursan of the Avian Science and Conservation Centre for assistance on all aspects of field work,
L. Volkov, N. Urbani, S. Perrot and H. Cunningham forlaboratory assistance, G. Maria for statistical help and J.
Briskie, T. R. Birkhead, I. Warkentin, B. Lemon, J. J. Negro,
J. L. Tella, P. Dunn, two anonymous referees and especially B. MacWhirter for constructive criticisms of thepaper. This study was supported by Infrastructure andOperating grants from the Natural Science and Engineering Research Council of Canada to D.M.B. and scholarships from the Province of Quebec Society for theProtection of Birds, a Chapman Award from the American
Museum of Natural History and a Sigma Xi grant to M.R.V.
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