Behavioral Ecology Vol. 12 No. 3: 340-347
© 2001 International Society for Behavioral Ecology
Experimental demonstration of the insurance value of extra eggs in an obligately siblicidal seabird
Department of Biology, Wake Forest University, Winston-Salem, NC 27109, USA
Address correspondence to L.D. Clifford. E-mail: cliffld5{at}wfu.edu .
Received 27 March 2000; revised 16 August 2000; accepted 22 September 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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A variety of organisms regularly produce more offspring than they raise. Despite the apparent energetic waste of such a reproductive tactic, overproduction may be favored by natural selection in some cases. One such case is when surplus offspring can serve as replacements, or insurance, for failed siblings. We tested the Insurance Egg Hypothesis (IEH) as an explanation for the overproduction of offspring in an obligately siblicidal seabird, the Nazca booby (Sula grant)i, which fledges a maximum of one nestling regardless of its clutch size. We manipulated clutch sizes within the range of natural variation encountered in this species (one-two eggs). The IEH predicts that parents with two-egg clutches should have higher reproductive success than those with one-egg clutches because the second egg can provide a nestling when the first egg fails to hatch, or when the first chick dies young. Consistent with the IEH, natural one-egg clutches that were enlarged to two eggs produced more hatchlings and fledglings than control one-egg clutches did, and natural two-egg clutches that were reduced to one egg produced fewer hatchlings and fledglings than control two-egg clutches did. We also evaluated aspects of the Individual Optimization Hypothesis, which proposes that individual optimal clutch sizes differ, as an explanation for clutch size variation in this species. In Nazca boobies, selection driven by replacement value appears to favor clutches larger than one even though final brood size is invariably one. One-egg clutches may be produced by parents experiencing some proximate limitation, such as a lack of food.
Key words: clutch size, Individual Optimization Hypothesis, Insurance Egg Hypothesis, Nazca booby, siblicide, Sula granti, surplus offspring.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Life history theory predicts that selection optimizes the cost-benefit relationships involved in clutch size evolution. An apparent paradox is presented by a variety of organisms that regularly produce more offspring than they can raise to maturity. For example, female coelacanths produce twice as many embryos as can be housed in their ovary; many parasitoid wasps lay large broods in a host from which only a single larva survives; and many female marsupials produce more young than the number of teats they have, resulting in the death of excess young (Mock and Parker, 1997
).
A number of avian species have an obligate brood reducing system (reviews
in Anderson, 1990a;
Mock et al., 1990) in which
surplus offspring are virtually always eliminated (> 95% of broods) through
substantial, overt sibling aggression
(Mock et al., 1990). Offspring
overproduction in these cases may have evolved to provide surplus offspring as
insurance against early failure of "core" offspring (number of
offspring that parents actually raise;
Mock and Forbes, 1995). The
Insurance Egg Hypothesis (Dorward,
1962) views production of excess young as an adaptation to
uncertain offspring viability (Anderson,
1990a).
Surplus offspring are thought to serve an insurance function in diverse
taxa (both obligately siblicidal and others) including angiosperms
(Ehrlén,
1991), beetles (Bartlett,
1987), parasitoid wasps
(Rosenheim and Hongkham,
1996), birds (e.g., Anderson,
1990a; Aparicio,
1997; Cash and Evans,
1986; Dorward,
1962; Forbes,
1990; Forbes et al.,
1997; Graves et al.,
1984; Hunt and Evans,
1997; Mock and Parker,
1986; Wiebe,
1996), and mammals (Anderson,
1990b; Millar,
1973; Mock and Parker,
1997). Theoretical studies provide robust support for the
insurance idea (Forbes, 1990;
Forbes and Lamey, 1996), and
several field studies indicate that surplus offspring can provide insurance
against failure of core offspring in some obligately siblicidal species,
increasing parental reproductive success as a result
(Anderson, 1990a;
Gargett, 1977;
Kepler, 1969). These field
studies were correlational, not experimental, so potentially confounding
variables were not controlled. For example, parents in better overall
condition might lay more eggs and take better care of offspring than do
parents in poor condition, leading to positive correlation of clutch size and
final reproductive success. Cash and Evans
(1986) conducted the lone
experimental test of the Insurance Egg Hypothesis (IEH) in an obligately
siblicidal species, using the American white pelican (Pelecanus
erythrorhynchos). They tested two predictions of the IEH and found
support for both.
If overproduction of offspring increases the reproductive success of
individuals within a species, then all individuals are expected to employ the
strategy. However, some individuals within obligately siblicidal species
produce only a single offspring. These individuals may experience constraints
that do not allow them to employ the overproduction strategy. Alternatively,
overproduction of offspring may not be the best strategy for all individuals
in a population. In other words, different individuals may have different
optimal clutch sizes (the Individual Optimization Hypothesis;
Högstedt,
1980; Perrins and Moss,
1975).
The Individual Optimization Hypothesis (IOH) was originally proposed in the
context of parents' varying abilities to provision broods of different sizes.
Previous tests of the IOH (e.g., Barber and
Evans, 1995; Nur,
1986; Pettifor,
1993; Pettifor et al.,
1988) have focused on the possibility that clutch size is adjusted
according to parents' ability to raise hatched offspring. Because obligate
siblicide typically occurs shortly after the second chick hatches, brood size
does not vary for the majority of the nestling period. However, costs may
accompany the incubation of the second egg, and the presence of the chick for
a short time before siblicide occurs, and therefore the IOH can be extended to
the incubation and laying period. In addition, if individuals produce eggs of
varying quality as suggested by Simmons
(1997), then two optimal
clutch sizes may exist, with high quality one-egg clutches producing highly
hatchable eggs, and lower quality two-egg clutches producing eggs of lower
hatchability but a similar probability of producing at least one
hatchling.
Here we derive predictions from both the IEH and IOH
(Table 1) and report an
experimental test of these hypotheses using an obligately siblicidal seabird,
the Nazca booby (Sula granti). The Nazca boobies of the
Galápagos have traditionally been considered
masked boobies (Sula dactylatra), but recent analyses of
morphological and breeding data (Pitman
and Jehl, 1998), and of mtDNA differentiation (Friesen et al.,
manuscript in review) support elevation of the
Galápagos and nearby populations to species
status. In this article we follow the nomenclature of Pitman and Jehl
(1998) and refer to these
birds as Nazca boobies. We did not test all aspects of the IOH and IEH, as we
were not able to force Nazca boobies to lay additional eggs or prevent them
from laying, and thus could not incorporate egg production and laying costs.
Our evaluation of these hypotheses is thus confined to the postlaying
period.
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Nazca boobies lay clutches of one or two eggs
(Nelson, 1966); over one
3-year period at our study site, 44-66% of clutches consisted of two eggs
(Anderson, 1990a). Eggs are
incubated for approximately 43 days, and eggs hatch about 5 days apart
(Anderson, 1993). If both eggs
hatch in a two-egg clutch, the first-hatched offspring pushes its sibling from
the nest scrape shortly after hatching, and it dies of exposure or is
scavenged by crabs or landbirds (Anderson,
1989; Nelson,
1978). Therefore, while clutch size varies among individuals,
final brood size does not. Chicks fledge at 113-120 days of age
(Nelson, 1978).
Nazca boobies provide a situation of unusual clarity for the study of
clutch size evolution. The obligately siblicidal nature of their brood-size
reduction results in surplus offspring having only replacement reproductive
value (Mock and Parker, 1986)
because it is only raised if the core offspring fails to hatch or dies very
early. The other component of reproductive value, extra reproductive value, is
that portion of the offspring's survivorship which is not contingent on the
fate of its sibling; it equals zero for Nazca boobies
(Mock and Parker, 1986).
Because most hypotheses for adaptive clutch size evolution focus on extra
reproductive value, they are not relevant in this case.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We conducted this experiment at the large breeding colony at Punta Cevallos, Isla Española, in the Galápagos Islands (1°20' S, 89°40' W; see Anderson and Ricklefs, 1987
) during the 1995-1996 breeding season
(October-June). On the first day of the experiment we used a pencil to mark
all eggs with a small "X," so that on subsequent days we could
identify newly-laid unmarked eggs. We checked for new clutches daily. When a
new clutch was found, we monitored it for 7-10 days to determine the natural
clutch size (laying intervals are 4-9 days; see
Anderson, 1993), before
assigning it to a treatment group. After this period, clutches were randomly
assigned (see below) to treatment groups and some clutch sizes were adjusted.
"Reduced" clutches had the second-laid "B-egg" removed
from natural two-egg clutches; "enlarged" clutches had a B-egg
added to natural one-egg clutches; and "switched" clutches
consisted of natural one-egg clutchs that were removed and replaced with a
single age-matched egg from another natural one-egg nest. The switched
treatment was designed to control for introduction of a foreign egg. In
addition, two control groups consisted of natural one-egg clutches (C1) and
natural two-egg clutches (C2). We assigned clutches to treatment groups with the objective of maintaining equal mean clutch initiation dates across treatments. However, one-egg clutches were less available (33.5% of clutches) and our experimental protocol required twice as many one-egg clutches as two-egg clutches. As a result, clutch initiation dates differed between some treatments. The median clutch initiation dates for the treatment groups were as follows: reduced, November 20 (n = 65); enlarged, November 20 (n = 57); C2, November 27 (n = 167); C1, November 27 (n = 36); switched one-egg clutches, December 6 (n = 60; Kruskall-Wallis H = 66.2, df = 4, p <.001). We were able to control statistically for differences in clutch initiation date (see Statistical Analyses). Natural two-egg clutches were assigned to the reduced group when a natural one-egg clutch was available to receive a donated egg and the donor's B-egg was 5-7 days younger than the recipient's A-egg, thereby mimicking natural laying asynchrony. Otherwise, two-egg clutches were assigned to the unmanipulated control group. One-egg clutches were assigned to the switched group when two natural one-egg clutches were laid within 2 days of each other. One-egg control clutches were treated identically, except that no eggs were exchanged.
We monitored nests daily to determine the fates of eggs and chicks. Because chicks from two-egg clutches hatch an average of 5 days apart, a distinct size difference between A- and B- chicks allowed us to distinguish between them. We weighed offspring every 10 days beginning on day of hatching (d 0) and continued until fledging, and when they reached an easily recognizable late developmental stage at which all but 1% of the down coverage had been replaced by pennaceous feathers.
Test of the Insurance Egg Hypothesis
The IEH assumes that B-eggs can provide an offspring when the A-egg fails
to hatch, or the A-offspring dies before siblicide occurs. Given the B-egg's
potential to act as insurance, the IEH predicts that two-egg Nazca booby
clutches should always yield higher reproductive success than do one-egg
clutches (Table 1). We first
examined the assumption that B-eggs provide a nestling when A-eggs fail or
A-chicks die. We tested the prediction of the IEH by comparing each group's
probability of producing at least one hatchling and probability of producing a
fledgling (fledging success). Fledging success may not accurately reflect
reproductive success if fledglings differ in quality. We therefore compared
offspring mass at the 1% down stage (see above) between groups, as well as
offspring growth rate.
Test of the Individual Optimization Hypothesis
The IOH assumes that individuals vary in quality. Clutch size may reflect
parental quality, with high quality parents producing larger clutches than low
quality parents do. This assumption is supported if parents that produce two
eggs have higher reproductive success than do parents that produce a single
egg. Given differences in parental quality, the IOH makes two directional
predictions in relation to our clutch size manipulations
(Table 1). Clutches which have
been adjusted by adding or removing an egg should have lower reproductive
success than control clutches do, because individuals should do best with the
clutch size that they laid. We tested the assumption and predictions of the
IOH by comparing the probability of producing at least one hatchling and the
probability of fledging between treatment groups.
Statistical tests
The first dependent variable of interest, whether or not a clutch produces
at least one hatchling, is a binary variable. Since Nazca boobies fledge a
maximum of one offspring per reproductive attempt, fledging success is also a
binary variable. Logistic regression is designed for use with dichotomous
dependent variables such as these, and allows the inclusion of a covariate. By
including clutch initiation date as a covariate, we were able remove variation
between experimental groups due to heterogenous clutch initiation dates, and
thus to examine variation due to experimental treatment alone. We initially
included clutch initiation date in the model as a continuous variable.
However, in checking the logistic regression assumptions, we found that the
logit transform did not linearize the probability of producing at least one
hatchling in relationship to clutch initiation date. When clutches were
divided into quartiles based on their clutch initiation dates, and the mean
probability of producing at least one hatchling for each quartile was plotted
against the clutch initiation date midpoint for each group, we found that the
probability of producing a hatchling remained constant over the first three
quartiles and dropped in the fourth quartile. The same pattern existed for
fledging success. This suggested treatment of clutch initiation date as a
dichotomous variable also (Hosmer and
Lemeshow, 1989): "early" if the clutch is initiated
during the first 75% of clutch initiation dates and "late" if
during the last 25%. We therefore constructed our models with two independent
variables: treatment and lay period (early or late).
When we examined interactions between treatment group and lay period for
the dependent variable fledging success, we found that the model including a
treatment by lay period interaction did not perform significantly better than
a model without the interaction (
2 = 3.50, df = 3, p
=.32). Therefore, we did not include a treatment by lay period interaction
term in our final model for fledging success. The model describing the
probability of producing at least one hatchling that included a treatment by
lay period interaction performed marginally better than the model without the
interaction term (2 = 5.67, df = 3, p =.13). This at
least suggested that the effect of treatment group did not remain constant
across levels of lay period. We therefore analyzed the probability of
producing at least one hatchling for early and late clutches separately.
Parameter estimates and probability levels were calculated using the
Statistica 4.5 nonlinear estimation module
(StatSoft Inc., 1993).
When testing for differences between treatment groups, we employed the
false discovery rate procedure (Benjamini
and Hochberg, 1995) to adjust p-values for multiple
comparisons. The procedure requires comparisons be ordered by decreasing
p-values, and then compared to a critical significance level
beginning with the largest p-value. The critical significance level
for each comparison, di, is calculated by dividing the
specific comparison number by the total number of comparisons and then
multiplying by the false discovery rate (the probability of mistakenly
rejecting a null hypothesis). For example, the fifth comparison (the
comparison with the fifth largest p-value) of six total comparisons,
given a false discovery rate of 0.05, has a di of 0.042 (=
5/6 * 0.05). If the achieved significance level is less than
di for a given comparison, then the null hypothesis is
rejected for that comparison, and all remaining comparisons
(Benjamini and Hochberg, 1995;
Curran-Everett, 2000).
To determine if offspring growth rates differed between treatment, we performed repeated measures ANCOVA on offspring masses measured at 10-day intervals for offspring that survived to fledging. We also analyzed offspring mass at fledging using ANCOVA.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Consequence of incubating a foreign egg
Enlarged clutches consisted of one egg that belonged to the parents and one foreign egg. If parents recognized the introduction of the foreign egg, they might have altered their incubation or attendance pattern, possibly affecting the probability of producing a hatchling. To evaluate this possibility, we compared the probability of producing at least one hatchling for one-egg control clutches, in which parents incubated their own egg, with switched clutches, in which parents incubated a single foreign egg. We initially performed logistic regression including lay period as a covariate, and found that the coefficient for lay period was not significant (t = 0.90, df = 93, p =.37), nor was the coefficient discriminating between the two groups (t = 1.29, df = 93, p =.20). Since the regression model indicated that lay period did not contribute significantly to the model, we performed a 2 x 2 contingency table analysis to compare the proportions of clutches that successfully initiated broods in these two groups (switched 24/60 = 0.40; C1 20/36 = 0.56) and found no significant difference (Yates' corrected
2 = 1.61, df = 1, p =.20),
indicating that parents incubating a foreign egg had the same probability of
producing at least one hatchling as did parents incubating their own egg. In
addition, an egg recognition experiment demonstrated that parents do not
discriminate their own 10 day old eggs from age-matched foreign eggs (Clifford
LD and Anderson DJ, unpublished data).
If parents did discriminate foreign eggs from their own and acted in a way
that lowered the probability of producing a hatchling, then we would expect
enlarged clutches (which contained a foreign egg) to have a lower probability
of producing at least one hatchling than C2 clutches did (which did not
contain a foreign egg). The proportion of enlarged clutches that produced at
least one hatchling (0.83, n = 57) was not lower than the proportion
in C2 clutches (0.77, n = 167; Yates's corrected 2 =
0.53, df = 1, p =.47), indicating that the presence of a foreign egg
in the nest did not alter the parents' behavior in a way that negatively
affected the probability of the foreign egg hatching. As a group, these
analyses indicated that the presence of a foreign egg in enlarged clutches did
not confound comparisons with treatment groups lacking foreign eggs. For the
remaining analyses, we used data from the C1 group, and not the switched
group, in order to be conservative in our comparisons.
Test of assumptions of the IEH
Final brood size was one in every nest that hatched two chicks. Most
B-chicks (97/103 = 0.942) were apparently ejected from the nest or died in the
nest within 6 days of hatching; all except one were dead by 15 days after
hatching. In that case the B-chick survived to 46 days. No parents produced
two fledglings.
The B-egg provided a hatchling when the A-egg failed to hatch in 8.8% (5/57) of enlarged clutches, and when the A-chick died in 3.5% (2/57) of enlarged clutches. The total replacement rate for enlarged clutches was 12.3% (7/57). In C2 clutches, the B-egg provided a hatchling when the A-egg failed to hatch in 8.4% (14/167) of clutches, and when the A-chick died in 1.2% (2/167) of clutches. The total replacement rate of B hatchlings for C2 clutches was 9.6% (16/167). The B-egg produced the surviving fledgling in 13.9% (5/36) of enlarged clutches that produced a fledgling, and in 10.5% (12/114) of C2 clutches that produced a fledgling in this experiment. Thus B-eggs had insurance value in both experimental and control broods.
Probability of producing a hatchling
The addition of treatment to a logistic regression model for early clutches
that included only the intercept significantly improved the model
(2 = 15.05, df = 3, p <.01), indicating that
membership in a treatment group influenced a clutch's probability of producing
at least one hatchling. For early clutches, the logistic regression model
describing the probability of producing a hatchling showed that C2 clutches
had a significantly higher probability of producing a hatchling than did
reduced or C1 clutches (Table
2). Enlarged clutches also had a significantly higher probability
of producing at least one hatchling than did reduced or C1 clutches. Enlarged
and C2 clutches did not differ in their probability of producing a hatchling,
nor did reduced and C1 clutches. These results supported all six of the IEH's
predictions, but only one of two predictions made by the IOH.
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The addition of treatment to a logistic regression model for late clutches
that included only the intercept did not improve the model (2
= 3.36, df = 3, p =.34), indicating that the probability of producing
at least one hatchling was not influenced by treatment in late clutches. The
probability of successfully initiating broods did not differ for any of the
treatments in late clutches (Table
2 and Figure 1).
Because of the small number of nests in the late lay period, power was less
than 80% to detect even a 50% difference between groups.
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Fledging success
Treatment group also significantly influenced a clutch's probability of
producing a fledgling (2 = 17.62, df = 1, p
<.001). Controlling for lay period, enlarged clutches had a significantly
higher probability of producing a fledgling than C1 clutches did
(Table 2). C2 clutches had a
marginally significantly higher probability of producing a fledgling than
reduced clutches did. C2 clutches had a significantly higher probability of
producing a fledgling than C1 clutches did, and reduced clutches had a
marginally significantly higher probability of producing a fledgling than C1
clutches did. The probability of producing a fledgling did not differ between
enlarged and reduced clutches, nor between enlarged and C2 clutches. Four of
the six predictions of the IEH and one of the two predictions of the IOH were
supported by these data.
Chick growth rates and mass at fledging
The growth rates of offspring that fledged in different treatment groups
did not differ from each other (F3, 164 = 0.872,
p =.46), and we detected no difference in offspring mass at the 1%
down stage across treatment groups (ANCOVA,F3, 192 = 0.83,
p = 0.48).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The Insurance Egg Hypothesis
The logistic regression model describing the probability of producing at least one hatchling for early clutches provided support for all six of the IEH's predictions. Nazca booby clutches with two eggs were more likely to produce a hatchling than were single-egg clutches, regardless of the parents' original clutch size (Figure 1). The C2, C1, and enlarged groups maintained their relationships to each other (Figure 1) in both the early and late clutch initiation periods, and they all had a lower probability of producing a hatchling late in the season. In contrast, the reduced group had approximately the same probability of producing a hatchling early in the season and late in the season (0.65 compared to 0.64).
While our data show an immediate effect of insurance eggs on the probability of producing at least one hatchling, data on fledging success better indicate whether the IEH is a sufficient ultimate explanation for variation in overall reproductive success among natural clutch sizes. Four of the six predictions of the IEH were supported by the fledging success data. Enlarged clutches had higher fledging success than C1 clutches did, indicating that parents that produced only one egg would have had higher reproductive success if they had laid two eggs. C2 clutches had higher fledging success than reduced clutches did, indicating that parents that produced two eggs would have had lower reproductive success had they produced only one egg. C2 clutches and enlarged clutches did not have significantly different fledging success, and C2 clutches had significantly higher fledging success than C1 clutches.
The logistic regression model for fledging success in Nazca boobies showed
a decrease in the probability of producing a fledgling late in the season that
paralleled the seasonal decline in the probability of producing a hatchling
(Figures 1 and
2). A seasonal decline in
reproductive success is a commonly observed pattern in birds and is associated
with a concomitant decrease in clutch size
(Crick et al., 1993;
Klomp, 1970;
Perrins, 1970). Our data
showed such a seasonal decline in reproductive success independent of clutch
size, since we saw a within-clutch size decrease in both the probability of
producing a hatchling and fledging success.
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The Individual Optimization Hypothesis
We found that parents laying two eggs were more successful at raising a
chick from hatching to fledging than were parents laying one egg. This result
supports the IOH's assumption of a positive correlation between clutch size
and parental quality. Reduced clutches had marginally significantly higher
fledging success than C1 clutches, and they fledged a similar proportion of
young to that of enlarged clutches. In both of these comparisons, it appears
that an additional effect on reproductive success interacts with the insurance
effect during the nestling period. The additional factor appears to involve
intrinsic parental quality. In the case of enlarged versus reduced clutches,
enlarged clutches had a significant advantage at hatching but not at fledging.
Parents of enlarged clutches originally laid only a single egg, and parents of
reduced clutches originally laid two eggs. Parents of enlarged clutches were
thus apparently less capable of finding food during egg formation, since food
limitation during this period accounts for most variation in clutch size
(Clifford LD and Anderson DJ, in
press). This variation in intrinsic parental quality was
associated with a marginally significant advantage of reduced parents over
enlarged parents in raising a hatchling to fledging among early layers (t =
1.91, df = 189, p =.057; Clifford LD and Anderson DJ, unpublished
data).
Differences in parents' abilities to produce a fledgling could result from
differences in abilities to absorb the costs of incubating additional eggs.
Some studies do suggest that incubation costs are reflected in the parents'
abilities to raise offspring (Heaney and
Monaghan, 1996; Monaghan and
Nager, 1997) and therefore affect fledging success and/or
offspring condition.
That parents producing large clutches are higher quality parents than those
producing small clutches has been suggested by correlations between clutch
size and offspring survival rate in other avian taxa (e.g., Kittiwake gull
Rissa tridactyla; Coulson and
Porter, 1985; Blue tit Parus caeruleus;
Nur, 1986). In addition,
experimental manipulations resulting in parents with the same brood sizes
showed that recruitment rates were higher for great tits (Parus
major) and blue tits (Parus caeruleus) that originally laid
larger clutches (Pettifor,
1993; Pettifor et al.,
1988), further indicating a quality difference between parents of
large and small clutches.
While our data did support the IOH's assumption that large clutches are produced by high quality parents, the critical test of the IOH is whether parents with manipulated clutch sizes have lower reproductive success than parents with unmanipulated clutch sizes. Experimentally enlarged clutches should have lower reproductive success than C1 clutches. This prediction is opposite that of the IEH, which predicts that enlarged clutches should have higher reproductive success than C1 clutches. Our data from Nazca boobies do not support this prediction of the IOH, as enlarged clutches had a higher probability of producing at least one hatchling as well as a higher probability of producing a fledgling than C1 clutches. Therefore, barring egg-laying costs and assuming that fledging success is an accurate estimate of parental fitness, Nazca boobies that lay one-egg clutches do not appear to be laying their optimal clutch size.
Parents with enlarged clutches were given "free" eggs without
incurring the cost of producing and laying them. These costs have been shown
to reduce chick survival and female condition in other species
(Heaney and Monaghan, 1995;
Monaghan et al., 1995,
1998). In addition, these
costs might affect parents' future survival or reproductive success
(Charnov and Krebs, 1974;
Williams, 1966). If we were
able to incorporate these costs into the experiment, we might find that the
optimal clutch size for some Nazca boobies was indeed one.
Insurance value and parental quality
In the early clutch initiation period, two-egg clutches had a clear
advantage over one-egg clutches in terms of the probability of producing at
least one hatchling. However, for clutches in the late clutch initiation
period, the logistic regression model failed to detect any significant
differences. This failure does not contradict the IEH for several reasons.
First, small sample sizes resulted in insufficient power to detect differences
of the magnitude observed. Second, while acknowledging low statistical power,
differences between the C2, C1, and enlarged were in the direction predicted
by the IEH. And last, clutches initiated in our "late" lay period
are of little significance to selection for clutch size because they represent
a small proportion of clutches (only 13.3% of 458 clutches laid by a random
sample of Nazca boobies in the Punta Cevallos colony were laid during this
same period) and late clutches have lower reproductive success than early
clutches do (Fernández P and Anderson DJ,
unpublished data).
Two of the predictions of the IEH were not supported by the fledging success data. Enlarged clutches had an insurance advantage at hatching (Table 2), but reduced clutches had a countervailing advantage in parental quality thereafter, so the two groups did not differ in overall fledging success (Table 2). We were able to experimentally decouple parental quality from clutch size; however, our estimate of parental quality will covary with clutch size in natural situations. Only two of the six predictions regarding fledging success in Table 2 do not confound clutch size and parental quality, and these constitute the essential test of the IEH, given our discovery of variation in parental quality. Both of these predictions (reduced versus C2 and enlarged versus C1) were strongly supported.
Variation in probability of producing a hatchling
In addition to parental quality differences between birds that laid
different clutch sizes, we also found an apparent within clutch size
quality difference reflected in hatching success (the proportion of eggs laid
that hatched). Enlarged clutches produced two hatchlings, one hatchling and
zero hatchlings at the frequency expected from a binomial expansion based on
hatching success (Table 3). For
example, the probability of two eggs hatching in an enlarged clutch is roughly
equal to (0.596) (0.596) = 0.355, the equivalent of 20 clutches in our sample.
The actual number of enlarged clutches that produced two hatchlings was 21.
But C2 clutches produced two hatchlings and zero hatchlings more often than
expected, and one hatchling less often than expected from the observed
hatching success. This indicates that some C2 parents produce two low quality
eggs or lose both more often than enlarged parents. This observation is
consistent with Nazca booby data reported by Anderson
(1990a), which showed that the
proportion of two-egg clutches in which either both hatched or both failed was
higher than expected if hatching was independent of nest. While these data
reflected only intrinsic hatchability, ours do not distinguish intrinsic
hatchability and extrinsic causes of egg loss.
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Other hypotheses for overproduction of offspring
Two other hypotheses have been proposed to explain overproduction of
offspring. The Resource Tracking Hypothesis (Lack,
1947,
1954;
Temme and Charnov, 1987)
proposes that surplus offspring serve a bet-hedging function; in years of high
resources they are raised in addition to core offspring, but in low resource
years they are eliminated. In 14 years of field work at the Punta Cevallos
colony, we have never seen parents raise two chicks to fledging (Anderson DJ,
unpublished data). Therefore this hypothesis is unlikely to explain two-egg
clutches. The Offspring Facilitation Hypothesis proposes that surplus
offspring aid core offspring to survive and/or reproduce
(Mock and Forbes, 1995), and
is commonly associated with cannibalism. However, Nazca booby B-chicks are not
consumed by conspecifics, nor do they offer any obvious aid to A-chicks.
The Insurance Egg Hypothesis appears to be the best explanation for
overproduction of offspring in the Nazca booby. We have shown that surplus
B-eggs can provide insurance against the failure of A-eggs. Experimentally
enlarged clutches produced more hatchlings and fledglings than control
clutches did, and experimentally reduced clutches produced fewer. Therefore,
selection should favor the production of two-egg clutches over one-egg
clutches, and one-egg clutches probably result from some proximate constraint
experienced by the parents. Evidence that females are limited by food
availability is provided by supplemental feeding experiments that increased
clutch size in birds (see reviews in Arcese
and Smith, 1988; Boutin,
1990; Martin,
1987; Meijer et al.,
1990; see also Aparicio,
1994; Nilsson,
1991; Soler and Soler,
1996), and litter size in mammals (review in
Boutin, 1990). Age may also
act as a proximate constraint; clutch size is known to increase with age in
many species (see review in Fowler,
1995).
The problem of unused insurance value is not unique to Nazca boobies; other
obligate brood reducing species also lay one-egg clutches, with varying
frequencies. For example, rock-hopper penguins (Eudyptes chrysocome)
apparently always lay insurance eggs
(Williams, 1981; but see
St. Clair and St. Clair,
1996), while several eagle species lay insurance eggs from 2-87%
of the time (Brown, 1966;
Cramp and Simmons, 1980;
Gargett, 1977;
Hustler and Howells, 1988;
Simmons, 1997). Future
experimental work, such as supplemental feeding, should attempt to identify
the causal factors preventing individuals from taking advantage of insurance
eggs in obligately siblicidal taxa with significant proportions of one-egg
clutches.
Insurance function has been most widely explored in obligately siblicidal
birds with small clutch sizes, but is also applicable to species that
experience less frequent offspring loss (Forbes,
1990,
1991;
Forbes et al., 1997;
Lamey et al., 1996;
Mock and Parker, 1986;
Mock et al., 1990). The
insurance reproductive value for last hatched nestlings in facultatively
siblicidal species can be equal to or greater than that found in obligately
siblicidal species (Wiebe,
1996). Brood size manipulations in the double-crested cormorant
(Phalacrocorax auritus), a facultatively siblicidal seabird that lays
clutches of three—four eggs, provided limited evidence that the
insurance value of eggs increased the reproductive success of parents
(Hunt and Evans, 1997).
However, fledging success for these broods was not ascertained. An
experimental test of the IEH in the lesser kestrel (Falco naumanni)
provided support for the IEH in a species that lays two—six eggs
(Aparicio, 1997). Other studies
have suggested that insurance is a contributing factor to clutch size
evolution in non-obligately siblicidal species with large clutch sizes
(Beissinger and Waltman, 1991;
Krebs, 1999). Future
considerations of clutch size evolution should not neglect the potential
insurance component of eggs and offspring.
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ACKNOWLEDGEMENTS |
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We thank the Galápagos National Park Service for permission to work in the park, and the Charles Darwin Research Station and TAME airline for logistical support. We thank B. Shelton, J. L. Norris, and D. Case for statistical assistance, M. R. Silman and L. S. Forbes for critical discussion of this topic, and S. R. Beissinger, K. P. Huyvaert, D. W. Mock, D. F. Westneat, and two anonymous reviewers for comments on an earlier version. National Science Foundation grant DEB93-04579 and DEB96-29539 and Wake Forest University provided financial support.
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