Behavioral Ecology Vol. 12 No. 1: 16-21
© 2001 International Society for Behavioral Ecology
Male boobies expel eggs when paternity is in doubt
Instituto de Ecología, Universidad Nacional Autónoma de México, A.P. 70-275, 04510 D.F., México
Address correspondence to M. Osorio-Beristain. E-mail: mosorio{at}miranda.ecologia.unam.mx .
Received 19 April 1999; revised 27 March 2000; accepted 17 May 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We analyzed the effect of increased risk of cuckoldry on male parental investment in eggs in the colonial blue-footed booby (Sula nebouxii). Seventeen experimental males were removed from the nesting territory for 10-12 h on a single day, 1-5 days before laying (females' supposed fertile period = SFP), and 17 control males were removed for the same amount of time on a single day, 7-29 days before laying (before the SFP). These removals were intended to simulate extended absence from the nest on a foraging excursion. Female extrapair courtship and copulation rates did not increase during the removal of the social mate, and there was no evidence that experimental and control males differed quantitatively in incubation or defense of the clutch. However, 43% of experimental males expelled the first-laid egg from the nest, whereas no control male did so. Apparently, male boobies drastically reduce parental investment in eggs with a presumed elevated probability of extrapair fertilization by destroying them.
Key words: expelling eggs, infanticide, paternity uncertainty, male parental investment.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Males of most marine bird species provide extensive parental care, involving incubation, feeding, and nest defense (Furness and Monaghan, 1987
).
However, studies of mating behavior and genetic parentage have shown that in
most species of marine birds some chicks are not descendants of the male
caregiver (Birkhead and Møller,
1992; Westneat et al.,
1990) and proportions of broods with multiple paternity vary from
0% in the northern fulmar (Fulmarus glacialis) and in Leach's
storm-petrel (Oceanodroma leucorhoa) to 18% in short-tailed
shearwater (Puffinus tenuirostris,
Westneat and Sherman, 1997).
That is, fertilization of eggs is not usually under complete control of the
male, and selection should therefore lead to the evolution of tactics whereby
males guard paternity (Trivers,
1972).
The risk of cuckoldry should result in an evolutionary arms race between
the cockolders and males being cuckolded, with females as important
participants (Smith, 1988).
Potential counter-adaptations include tactics before females lay, such as
mate-guarding (Parker, 1970,
1974), frequent copulations to
dilute the sperm of other males (Parker,
1974), copulation delay
(Erickson and Zenone, 1972),
and sperm removal (Davies,
1983). Tactics after females lay include mate desertion and
provision of parental care by the male in proportion to relative certainty of
paternity (Trivers, 1972;
Westneat and Sherman, 1993).
Males that desert have less time and opportunity to find a mate and breed
during the season and remating would involve additional costs of courtship,
copulations, nest building, and territorial defense
(Smith, 1988;
Westneat and Sherman, 1993).
As a result, providing parental care at a level proportional to certainty of
paternity (perception of paternity;
Schwagmeyer and Mock, 1993)
could be less costly than desertion, particularly if the male can reduce his
investment in offspring of uncertain paternity early during the period of
parental care (cf. Robertson,
1990; Rohwer,
1986). When their share of paternity is lower, males can also
provide less food to the brood (Dixon et
al., 1994). As far as we know, they are not able to discriminate
their own chicks within a brood and feed them preferentially
(Westneat et al., 1995;
Westneat and Sargent,
1996).
To test whether males provide care in proportion to their perceived
paternity, it is necessary to experimentally manipulate perceived paternity
(Kempenaers and Sheldon,
1997). Hitherto, most attempts at doing this by temporarily
removing males or females during the presumed fertile period have failed to
reveal an effect (reviews in Kempenaers et
al., 1998; Westneat and
Sargent, 1996; Wright and
Cotton, 1994). However, only terrestrial species have been tested,
such as barn swallows (Hirundo rustica; Møller,
1988,
1990), tree swallows
(Tachycineta bicolor, Whittingham
et al., 1993), dunnocks (Prunella modularis;
Davies et al., 1992), alpine
accentors (P. collaris; Hartley
et al., 1995), and acorn woodpeckers (Melanerpes
formicivorus; Koenig,
1990). Here, we report the first test using a colonial marine
bird.
We tested the prediction that male parental care should decrease as uncertainty of paternity increases in the socially monogamous blue-footed booby (Sula nebouxii). We attempted to reduce the certainty of paternity of 17 experimental males by removing them from their mate for 10-12 h, on a single day 1-5 days before laying, and compared their mate guarding, paternity guarding, incubation, and nest defense behavior with 17 control males that were separated from their mates for the same amount of time 7-29 days before laying.
Under natural conditions, during the 1-5 days before female blue-footed
boobies begin laying, they exhibit their highest rate of extrapair copulations
in absence of their mates, at the same time that both partners are exhibiting
their highest rates of attendance, intrapair courtship and intrapair
copulations (Osorio-Beristain and
Drummond, 1998). Partners copulate only on their own territory,
and extrapair copulations occur there also, or within a few meters (personal
observation). Male attendance is associated with decreased extrapair activity
by their social mates, and hence probably serves a mate-guarding function, as
may their intrapair courtship
(Osorio-Beristain and Drummond,
1998). Frequent copulation by male social mates during the 5 days
before laying could function as a paternity guard. By removing the
experimental males during this period, the experiment simulated extension of
natural male foraging absences that normally would not last more than 3.5 h
(Osorio-Beristain and Drummond,
1998), thereby decreasing the opportunity for mate guarding and
paternity guarding. We reasoned that increased absence should decrease the
perception of certainty of paternity in experimental males more than in
control males. In addition, we predicted that female extrapair behavior (rates
of courtship and copulation) should increase in response to decreased guarding
by males.
Male blue-footed boobies share with their mate all parental care duties
from the time the first egg is laid until chicks fledge
(Nelson, 1978), and both
adults frequently depart from the nest site for presumed foraging trips
(Osorio-Beristain and Drummond,
1998). Males and females apparently differ little in their
contribution to incubation, brooding, nest attendance and nest defense,
although females provide considerably more food than males
(Guerra and Drummond, 1995).
The incubation period is 40 days and chicks are fed for more than 140 days
(Torres and Drummond, in press), hence successful reproduction requires
extensive cooperation and coordination of the sexes.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Between 15 January and 16 March, 1995, we observed mated pairs of blue-footed boobies nesting in high density areas at the forest edge by the Northeast and Southwest shores of Isla Isabel, Mexico. All birds were individually leg-banded and had nested in at least one previous season.
We observed 34 focal pairs from four canvas blinds, in which two observers alternated 2 h shifts, watching a maximum of eight focal pairs. Birds were considered a pair if they courted each other and both defended a territory in which they eventually incubated a clutch. Every territory was marked with a numbered peg when the pair was absent.
Experimental design
We removed 17 randomly chosen experimental males 1-5 days before their mate
laid its first egg (mean ± SD, 3.65 ± 1.03 days) and also
removed 17 randomly chosen control males 7-29 days before laying (15.47
± 6.49 days). All males were captured between 0600 and 0800 h, and
released in the late afternoon after 11.07 ± 0.57 h for experimental
males, and 11.12 ± 0.43 h for control males (range = 10-12 h,
n = 34 experimental and control males). Experimental males were
removed when the cloaca of their social partner was open and reddish,
indicating proximity of laying of the first egg (personal observation).
Control males were removed when the cloaca of their social partner was closed
and not reddish.
Dates of removal for both experimental and control males were similar: from 1 February to 3 March in experimental males, and from 28 January to 8 March in control males (D = 0.03, p = 1.00, Kolmogorov-Smirnov test, n = 17 males of each treatment). To assess the body condition of experimental and control males at the beginning of the reproductive period, we measured body mass (g) and culmen and left ulna length (mm) at the time the birds were captured for removal. There was no significant difference in body condition of experimental and control males (Table 1).
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Males were held in individual (70 x 70 cm) floorless metallic cages approximately 100 m from their nesting territory. At this distance, and given the noise from waves and the colony, it is unlikely that the males heard their mates during captivity. Each cage was covered with a white cotton cloth to reduce external stimulation. Males spent their captivity apparently relaxed, sleeping and standing on the ground. When males were released at twilight by lifting the cage, they flew out to sea and during our 30 min watch did not return to their nests. Every male was on its territory next morning at 0600 h.
Behavioral observations
Daily behavioral observations were made from 0800 to 1800 h. Courtship
occurred when two interacting birds performed any of these displays: sky
pointing, parading, symbolic nest building, or bill-up-face-away
(Nelson, 1978). We recorded a
copulation whenever a male stood on a female's back and either the cloaca of
the two birds came into contact or, if the cloacae were out of sight, the
female rotated and elevated her tail and the male simultaneously rotated and
lowered his tail down to the ground
(Osorio-Beristain and Drummond,
1998).
Female promiscuity
We observed the behavior of experimental and control females the day before
removal of their mates, the day of removal itself and the day after removal.
We recorded the absolute frequency of copulations, and, during each 15 min
interval throughout the observation period, whether the focal female engaged
in reciprocal courtship with a male (one-zero record). We compared frequencies
during the day that the male was removed with the average of the frequencies
on the days before and after removal.
Mate guarding and paternity guarding by males
Each experimental male was observed the day after its removal; each control
male was observed from the day after its removal until the day its mate laid
the first egg. At 15 min intervals throughout the observation period, we noted
the presence or absence of both partners of each focal pair, whether the male
engaged in reciprocal courtship with his mate (one-zero record), and the
absolute frequency of intrapair copulations.
We analyzed male behavior by matching each experimental male with a control male, and comparing courtship and copulation rates on the same day of the social partner's reproductive cycle, calculated as the number of days prior to the laying of the first egg. The day of comparison was the day after each experimental male's removal. We matched each experimental male with the control male that bred closest in nest location and also closest to the date of laying of the social partner's first egg. In total we matched 12 pairs of experimental-control males. Five pairs of males could not be compared because their mobility prevented us observing them during part of the observation period.
Male parental care
Incubation
We recorded the date and hour that each focal female laid her first egg. We
observed each male's behavior during the first hour of its first incubation
shift and we noted if the male covered the first egg, or exhibited any obvious
behavior indicating an unwillingness to incubate. Additionally, from the time
that the first egg was laid until the third egg was laid (or for 5 days after
the second egg was laid if only two eggs were laid), we recorded whether the
clutch was covered by the male or by the female at 15 min intervals throughout
the observation periods. For the analysis of incubation periods, we only
included clutches of one egg: either the first egg or the second egg in cases
where the first had disappeared (by predation or breaking by neighboring
birds), and only clutches where the egg survived more than 1 h. During the
1995 reproductive season, booby eggs were frequently predated by Heermann's
gulls (Larus heermanni), probably because of reduction in the
availability of marine foods associated with an El
Niño oceanographic event
(Trenberth and Hoar,
1996).
Clutch defense
We recorded the intensity of the male's defense of the clutch against a
standardized event of human intrusion. Each intrusion was performed when the
male was incubating the clutch and his mate was absent. Two people slowly and
silently walked toward the clutch in single file, approximately 50 cm apart,
looking at the bird's eyes. The second person in line stopped 3 m from the
nest and recorded the male's behavior. The first person stopped 30 cm from the
nest for 30 s. If the male did not uncover the clutch during this period, then
the person gently pushed the bird off the clutch with a stick. We verified
that each bird returned and covered the clutch after the test. No clutch was
lost or abandoned as a result of this test.
The intensity of male defense was ranked in four exclusive categories based on whether the clutch was uncovered while: (1) the intruder walked toward the nest at a distance greater than 30 cm; (2) the intruder stood 30 cm from the clutch during 30 s; (3) the bird was pushed off the clutch without attacking; or (4) the bird attacked the stick with its beak while being pushed. These categories were, respectively, assigned one, two, three, or four points on a scale of increasing intensity.
We performed the intrusion to clutches of one and two eggs (1.50 ± 0.46 eggs, n = 10 experimental males; 1.70 ± 0.50 eggs, n = 9 control males; U = 48, p =.23, Mann-Whitney U test). The age of the first egg in the clutch was similar in experimental (22.33 ± 10.37, range = 8-38 days) and control males (20.9 ± 9.49, range = 6-34 days; U = 58, p =.92, Mann-Whitney U test). The time of day during which the probe was made did not differ between experimental (1050 ± 0350, range = 0801-1733 h) and control males (0918 ± 0243, range = 0751-1720 h; U = 39, p =.18, Mann-Whitney U test).
Inter-observer reliability
Tests of inter-observer reliability were carried out throughout the study
by having two observers independently record six focal pairs during an average
of 27.54 ± 3.54 h per pair. The average difference between two
observers was 6.2% for records of copulation frequency (± 8.7%, range =
0.0-25.0%), 8.7% for records of courtship during 15 min intervals (±
3.6%, range = 2.5-15.0%) and 4.5% for records of presence/absence of each
focal bird (± 5.3%, range = 2.2-13.5%).
All statistical tests are two-tailed, and data values given in the text are mean ± SD.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Female promiscuity
Contrary to our prediction, neither experimental nor control females exhibited higher reciprocal extrapair courtship rates on the day their mate was removed than on the average of the days bracketing removal (Table 2). Indeed, on the day that males were removed, courtship rates declined 2.7 and 1.2 times in the samples of experimental and control females, respectively, in comparison to the days that bracketed removal. Extrapair courtship was performed by eight of 17 experimental females and six of 17 control females; propensity to perform this activity did not differ between females in the two treatments (p =.73, Fisher's exact probability test).
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Neither experimental nor control females exhibited significantly higher extrapair copulation rates during their mate's removal than they did before and after the removal (Table 2). Extrapair copulations were performed by two of 17 experimental females and three of 17 control females; propensity for promiscuity was similar between females in the two treatments (p = 1.00, Fisher's exact probability test). Latency to copulate with another male after separation from their mate was similar in experimental females (2.50 ± 0.62 h) and control females (2.96 ± 0.88 h).
Only experimental and control females that had exhibited extrapair courtship during 1-15 days before the removal of their mate (n = 14 females) performed extrapair courtship during the removal. No experimental or control female that had not exhibited extrapair courtship on the days before the removal of their mate (10.65 ± 6.11 days of observation, range = 7-29 days; n = 20 females) performed extrapair courtship during his absence.
Mate guarding and paternity guarding by males
Experimental males did not differ significantly from controls in frequency
of presumed mate guarding and paternity guarding behaviors (female attendance,
intrapair courtship and intrapair copulation) following their return to the
nest (Table 3). Nor was there
any firm evidence that males increased their attendance or intrapair
copulations in response to the removal: Their increase in attendance (day
after minus day before) was 0.17 ± 0.21 h compared to an increase of
0.13 ± 0.29 h in control males over the same period (U = 87,
p =.40, n = 12, Mann-Whitney test), and their increase in
copulations was 0.25 ± 0.75 compared to an increase of 0.10 ±
0.67 in control males over the same period (U = 82, p =.58,
n = 12, Mann-Whitney test).
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Male parental care
One of 17 experimental males did not incubate the first egg because his
partner laid the egg in a neighboring nest while both neighbors were absent.
The neighbors returned 2.25 h later, promptly defended their nest (with the
egg) and went on to incubate the egg until it hatched. Hence, this
experimental male was deleted from the analysis of egg expulsion (see
below).
Consistent with the prediction that male parental care should decrease in response to increased uncertainty of paternity, 43.7% of 16 experimental males expelled their social partner's first egg from the nest without incubating it, while none of 17 control males did so (p =.007, Fisher's exact probability test). Infanticidal males expelled the egg minutes after they assumed their first incubation shift. The experimental males' first incubation shift occurred 2.23 ± 1.64 h after the first egg was laid (range = 0.25-5.25 h). These seven males carried the egg away from the nest in their mandibles or rolled it out of the nest (to a distance of 30-40 cm from the nest) by pushing with the culmen. In two cases, the female was standing within 1 m of the nest while the male was expelling the egg, but neither female exhibited any obvious behavior to prevent expulsion. The other five females were absent from the observation area when their eggs were expelled. All control and experimental females were present when males first started incubation. Of the seven eggs that were expelled, three were subsequently broken by neighbors, two were predated by gulls, and we collected and preserved the remaining two before they could be destroyed.
We looked for differences between the seven experimental birds that ejected
eggs and the nine experimental birds that did not, that might account for the
infanticidal behavior. We did not find differences in behavior (intrapair
courtship and copulations), body size (weight, culmen, and ulna length) or
nesting context (distance between neighbors)
(Table 4). Furthermore, the
probability of extrapair activity during the absence of the mate did not
differ between experimental females in pairs where the first egg was
eliminated (two of seven females) and those in pairs where it was not
eliminated (six of nine females) (p =.31, Fisher's exact probability
test). Nor was there a clear relationship between timing of male removal and
probability of egg expulsion (logistic regression: 
2 = 3.53,
df = 1, p =.06).
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Incubation
For experimental males that did not expel the egg, we examined the
investment they made in incubation. Experimental and control males incubated
the first egg for similar proportions of time (measured as the proportion of
the total incubation time contributed by both partners to each clutch) :
experimental males (0.30 ± 0.17; n = 5 first egg clutches) and
control males (0.34 ± 0.22; n = 8 first egg clutches)
(U = 11, p =.84, Mann-Whitney U test).
Five experimental and nine control males lost their first egg to gull predation, so we repeated the analysis including the incubation data of the second egg in clutches where the first egg had disappeared due to predation or had been expelled by males. The analysis included the total period that the single egg (the first or the second) survived alone in the nest. Both experimental and control males incubated clutches of one egg for similar proportions of time: experimental males, 0.38 ± 0.11 (n = 5 first egg clutches, 8 second egg clutches), control males, 0.32 ± 0.26 (n = 8 first egg clutches, 1 second egg clutch; U = 13, p =.79, Mann-Whitney U test).
Clutch defense
The measure of intensity of nest defense did not differ between
experimental males (3.10 ± 1.76, n = 10) and control males
(2.42 ± 1.55, n = 9; U = 46.5, p =.42,
Mann-Whitney U test).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Contrary to expectation, females did not increase extrapair behavior during the experimental absence of their social mate. It is noteworthy that only females that had performed copulations or courtship with an extrapair mate before removal of their social mates (14/34 experimental and control females) performed promiscuous behavior during the 11-hour period of removal. Hence, the selective extrapair behavior of females (cf. Kempenaers et al., 1992
;
Sheldon, 1994) was apparently
unaffected by the experimental absence of their social mates. This is
surprising because extrapair behavior of female blue-footed boobies is
generally greater in the absence of the social mate
(Osorio-Beristain and Drummond,
1998). Possibly the procedure of capturing males at the nest site
disturbed females and somehow discouraged their extrapair behavior during the
rest of the day. In any event, our experimental design did not require
increased extrapair behavior by females, but rather perception by males of
increased female opportunity for extrapair behavior (cf.
Kempenaers and Sheldon, 1998;
Lifjeld et al., 1998).
Although other interpretations are possible, our data support Trivers'
(1972) hypothesis that males
should adjust their level of parental investment according to their perception
of certainty of paternity (see Schwagmeyer
and Mock, 1993). The manner of adjustment was unexpected, drastic
and as far as we know unique. Rather than quantitatively reducing their
investment in incubation and defense of the clutch, 43% of 16 experimental
males (versus 0% of 17 control males) expelled the first-laid egg.
Subsequently, they defended and incubated the remaining clutch with behavior
similar to control male behavior. We infer that the first-laid egg was
destroyed because of the heightened probability that it was fertilized by an
extra mate, although paternity has not been analyzed and this probability is
unknown. Isolating and targeting just the first-laid egg implies that
paternity of later-laid eggs was not threatened by female extrapair
copulations in the 5 days before start of laying. This is consistent with the
observation that after laying the first egg females continue copulating with
their social mates but not their extra mates before laying their next eggs
(Osorio-Beristain and Drummond,
1998).
Expulsion of eggs by experimental males but not control males is evidence
that the timing of male removal was the critical variable determining
expulsion. Descriptive behavioral data are consistent with female fertility
being high during the 5 days before laying: Apparent mate guarding and
paternity guarding by males (attendance combined with courtship and
copulation) and extrapair behavior of females peak then, and females
apparently decline to perform extra pair copulations in the social mate's
presence (Osorio-Beristain and Drummond,
1998). Males destroyed eggs only when their forced absence
coincided with the time when their social mates were presumably most
vulnerable to fertilization by another male. It could be argued that capture
and detention of males induced a pathological destruction of eggs, affecting
only experimental males because their social mates laid shortly after the
manipulation. This seems unlikely since egg expulsion occurred 3-5 days after
the manipulation (giving time for recovery from the trauma of capture), but we
cannot discount the possibility that removal disturbed the hormone levels and
subsequent behavior of males.
Experimental removal of males and females of other species to reduce male
certainty of paternity has not led to males selectively destroying eggs.
However, in the tested species (dunnocks, alpine accentors, barn swallows,
tree swallows, and eastern bluebirds) males do not incubate and may have no
opportunity to selectively destroy an egg. Maybe this option is available only
when males incubate shortly after the laying of each suspect egg. In the
cooperatively breeding acorn woodpecker, males do participate in incubation
and are apparently capable of non-selective egg destruction. Two of eight
males removed during laying subsequently expelled all eggs from the nest,
whereas none of seven control males did so
(Koenig and Mumme, 1987).
Infanticidal behavior (of eggs and chicks) by males of other avian species
occurred in a mate switching context, where a male was replaced by another
male (Crook and Shields, 1985;
Freed, 1986,
1987;
Pinxten et al., 1991;
Robertson, 1990;
Robertson and Stutchbury,
1988; Veiga, 1990;
review in Smith et al., 1996).
Infanticide by the replacement male is clearly adaptive when replacement
occurs during the incubation or nestling stages
(Robertson, 1990;
Robertson and Stutchbury,
1988). Infanticidal egg expulsion by male boobies shows greater
behavioral complexity, occurring as it does a few days after an event defined
by quantitative features (e.g., timing and duration).
Adaptive reduction of male parental investment when probability of
paternity is low depends on the availability of reliable paternity cues to the
male. Our results imply that the cues used by male blue-footed boobies involve
absence of the male from the nest site and from the social mate and proximity
to time of laying. This is certainly consistent with females generally
performing far more extrapair copulations during absences of their social
mates (Osorio-Beristain and Drummond,
1998). To date, paternity cues have been identified for only two
avian species, both of which breed cooperatively: The dunnock
(Davies, 1992;
Davies et al., 1992) and the
accentor (Hartley et al.,
1995). Paternity cues in these congeners are related to the amount
of time the male spends near the female during her fertile period: In broods
where two males provide parental care simultaneously, males care in proportion
to their copulatory access time. In all three species the cue utilized may be
directly related to the caretaking male's probability of siring the affected
offspring. Demonstration of this relationship in blue-footed boobies will of
course require analysis of paternity.
Although our experiment suggests that the male's decision to destroy the first-laid egg depends on its opportunity to guard the social mate when she is most fertile, we should suspect that additional factors are involved. Nine of 16 experimental males did not expel the first-laid egg. There was no evidence that these non-expellers differed from expellers in body condition or in frequency of mate guarding and paternity guarding behavior after removal; nor was there evidence that their social mates were more likely to perform extrapair activity during experimental removal than the social mates of expellers. Our small samples do not allow us to dismiss these plausible paternity cues, and other cues are also possible.
Selective destruction of the first-laid egg should benefit males only when the probability of extrapair fertilization is high or if females respond to destruction by laying a replacement egg with a lower probability of extrapair fertilization. Unfortunately, we have no information on paternity and the high rates of egg predation by Heermann's gulls during our experiment prevent us from analyzing whether replacement eggs were laid.
Do blue-footed booby males destroy eggs in the natural context? We recorded two instances in nests observed daily during all daylight hours at the Isla Isable colony, in 1996 (unpublished data). During the 5 days before start of laying, the females courted with an extra male in their social mate's presence and copulated with the extra male in his absence. In both cases, the male social mate destroyed the first-laid egg at the start of his first incubation stint, one by pushing it out of the nest (where a gull subsequently predated it) and the other by piercing it with the bill. First egg destruction by male boobies is a natural behavior and our experiment shows that it is likely to occur when the male has been extensively absent during precisely the period when females are assumed to be most fertile.
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ACKNOWLEDGEMENTS |
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This article is based on M.O.-B.'s Ph.D. thesis at the Instituto de Ecología, Universidad Nacional Autónoma de México (UNAM). Field work was supported by UNAM, CONACyT grant 4722-N9407 to H.D., and a student fellowship to M.O.-B. We thank A. Hernández, E. Delgado, L. Terrazas, A. García, and J. Martínez for help with field work. The Mexican Navy provided transportation and logistical support. The fishermen of San Blas and Boca de Camichín, Nayarít, also provided logistical support. M.O.-B. thanks J. Martínez, J.L. Osorno, W. Reid, L. Eguiarte, W. Eberhard, and C. Macías for multiple comments on this work at different stages.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Birkhead TR, Møller AP, 1992. Sperm competition in birds: evolutionary causes and consequences. London: Academic Press.
Crook JR, Shields WM, 1985. Sexually selected infanticide by adult male barn swallows. Anim Behav 33: 754-761.
Davies NB, 1983. Polyandry, cloaca-pecking and sperm competition in dunnocks. Nature 302: 334-336.
Davies NB, 1992. Dunnock behavior and social evolution. Oxford series in ecology and evolution. Oxford: Oxford University Press.
Davies NB, Hatchwell BJ, Robson T, Burke T, 1992. Paternity and parental effort in dunnock Prunella modularis: how good are males' chick-feeding rules? Anim Behav 43: 729-745.
Dixon A, Ross D, O'Malley SLC, Burke T, 1994. Paternal investment inversely related to degree of extra-pair paternity in the reed bunting. Nature 371: 698-700.
Erickson CJ, Zenone PG, 1972. Courtship differences in male ring doves avoidance of cuckoldry? Science 192: 1353-1354.
Freed LA, 1986. Territory takeover and sexually selected infanticide in tropical house wrens. Behav Ecol Sociobiol 19: 197-206.
Freed LA, 1987. Prospective infanticide and protection of paternity in tropical house wrens. Am Nat 130: 948-954.
Furness RW, Monaghan P, 1987. Seabird ecology. New York: Chapman and Hall.
Guerra M, Drummond H, 1995. Reversed sexual dimorphism and parental care: minimal division of labour in the blue-footed booby. Behaviour 132: 479-496.
Hartley LR, Davies NB, Hatchwell BJ, Desrochers A, Nebel D, Burke T, 1995. The polygynandrous mating system of alpine accentor, Prunella collaris, vol II. Multiple paternity and parental effort. Anim Behav 49: 789-803.
Kempenaers B, Lanctot RB, Robertson RJ, 1998. Certainty of paternity and aternal investment in eastern blue birds and tree swallows. Anim Behav 53: 423-427.
Kempenaers B, Sheldon BC, 1997. Studying paternity and paternal care: pitfalls and problems. Anim Behav 55: 845-860.
Kempenaers B, Sheldon BC, 1998. Confounded correlations: a reply to Lifjeld et al. and Wagner et al. Anim Behav 55: 241-244.[ISI][Medline]
Kempenaers B, Verheyen GR, Dhondt AA, 1992. Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol Sociobiol 5: 481-492.
Koenig WD, 1990. Opportunity of parentage and nest
destruction in polyandrus acorn woodpeckers, Melanerpes formicivorus.
Behav Ecol 1:
55-61.
Koenig WD, Mumme RL, 1987. Population ecology of the cooperatively breeding acorn wood pecker. Princeton, New Jersey: Princeton University Press.
Lifjeld JT, Anthonisen K, Blomqvist D, Johnsen A, Krokene C, Rigstad K, 1998. Studying the influence of paternity on paternal effort: a comment on Kempenaers & Sheldon. Anim. Behav 55: 235-238.[ISI][Medline]
Møller AP, 1988. Paternity and parental care in the swallow, Hirundo rustica. Anim Behav 36: 996-1005.
Møller AP, 1990. Defence of offspring of male swallow, Hirundo rustica, in relation to participation in extra-pair copulations by their mates. Anim Behav 42: 261-267.
Nelson J B, 1978. The sulidae: gannets and boobies. Oxford: Oxford University Press.
Osorio-Beristain M, Drummond H, 1998. Non-aggressive mate guarding by the blue-footed booby: a balance of female and male control. Behav Ecol Sociobiol 43: 307-315.
Parker GA, 1970. Sperm competition and its evolutionary consequences in the insects. Biol Rev 45: 525-567.
Parker GA, 1974. Courtship persistence and female guarding as male time investment strategies. Behaviour 48: 157-184.
Pinxten R, Eens M, Verheyen RF, 1991. Responses of male starlings to experimental intraspecific brood parasitism. Anim Behav 42: 1028-1030.
Robertson RJ, 1990. Tactics and counter-tactics of sexually selected infanticide in tree swallows. In: Population biology of passerine birds (Blondel JB, Goler A, Lebreton JD, McCleery R, eds) Berlin: Springer-Verlag; 381-390.
Robertson RJ, Stutchbury BJ, 1988. Experimental evidence for sexually selected infanticide in tree swallows. Anim Behav 36: 749-753.
Rohwer S, 1986. Selection for adoption versus infanticide by replacement mate in birds. In: Current Ornithol, vol. 3 (Johnston R, ed). New York: Plenum Press; 353-395.
Schwagmeyer PL, Mock DW, 1993. Shaken confidence of paternity. Anim Behav 46: 1020-1022.
Sheldon BC, 1994. Male phenotype, fertility and the pursuit of extrapair copulations by female birds. Proc R Soc Lond B 257: 25-30.
Smith SM, 1988. Extra-pair copulations in black-capped chickadees: the role of the female. Behaviour 107: 15-23.
Smith HG, Wennerberg L, von Schantz T, 1996. Adoption or infanticide: options of replacement males in the european starling. Behav Ecol Sociobiol 38: 191-197.
Torres R, Drummond H, 1999. Does large size make daughters of the blue-footed boody more expensive than sons? J Anim Ecol 68: 1133-1141.
Trenberth KE, Hoar TJ, 1996. The 1990-1995 El Niño-southern oscillation event: longest on record. Geophys Res Lett 23: 57-60.
Trivers R, 1972. Parental investment and sexual selection. In: Sexual selection cnd the descent of man 1871-1971 (Cambell B, ed). Chicago: Aldhine; 36-179.
Veiga JP, 1990. Infanticide by male and female house sparrow. Anim Behav 39: 496-502.
Westneat DF, Clark AB, Rambo KC, 1995. Within-brood patterns of paternity and paternal behavior in red-winged blackbirds. Behav Ecol Sociobiol 37: 349-356.
Westneat DF, Sargent RC, 1996. Sex and parenting: the effects of sexual conflict and parentage on parental strategies. Trends Ecol Evol 11: 87-91.
Westneat DF, Sherman PW, 1993. Parentage and the
evolution of parental behaviour. Behav Ecol
4: 49-60.
Westneat DF, Sherman PW, 1997. Density and extra-pair fertilizations in birds: a comparative analysis. Behav Ecol Sociobiol 41: 205-215.
Westneat DF, Sherman PW, Morton M L, 1990. The ecology and evolution of extra-pair copulations in birds. In: Current Ornithol, vol 7 (Power MD, ed). New York: Plenum Press; 331-369.
Whittingham LA, Dunn PO, Robertson RJ, 1993. Confidence of paternity and male parental care: an experimental study in tree swallows. Anim Behav 46: 139-147.
Wright J, Cotton PA, 1994. Experimentally induced sex differences in parental care: an effect of certainty of peternity? Anim Behav 47: 1311-1322.
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