Behavioral Ecology Vol. 12 No. 3: 340–347 Experimental demonstration of the insurance value of extra eggs in an obligately siblicidal seabird L. D. Clifford and D. J. Anderson Department of Biology, Wake Forest University, Winston-Salem, NC 27109, USA 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 granti), 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. [Behav Ecol 12:340–347 (2001)] L ife 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, Address correspondence to L.D. Clifford. E-mail: [email protected] Received 27 March 2000; revised 16 August 2000; accepted 22 September 2000. 2001 International Society for Behavioral Ecology 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 there- Clifford and Anderson • Insurance eggs in boobies Table 1 Predictions and assumptions of the Insurance Egg Hypothesis (IEH) and Individual Optimization Hypothesis (IOH) with respect to experimental treatment groups, with inequalities indicating which treatment groups should have a higher probability of producing at least one hatchling and a higher probability of producing a fledgling in pairwise comparisons Insurance Egg Hypothesis Individual Optimization Hypothesis Predictions Predictions Reduced ⬍ control 2 Enlarged ⬎ control 1 Reduced ⬍ control 2 Enlarged ⬍ control 1 Reduced ⫽ control 1 Reduced ⬍ enlarged Enlarged ⫽ control 2 Control 2 ⬎ control 1 Reduced ⬎ control 1 Reduced ⬎ enlarged Enlarged ⬍ control 2 Control 2 ⬎ control 1 Assumptions The critical prediction distinguishing the two hypotheses appears in bold type. fore 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. 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 evo- 341 lution focus on extra reproductive value, they are not relevant in this case. METHODS 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 clutches 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 Bchicks 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 pro- Behavioral Ecology Vol. 12 No. 3 342 ducing 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. RESULTS 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 ⫻ 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. Clifford and Anderson • Insurance eggs in boobies 343 Table 2 Predicted probabilities and significance tests from logistic regression models describing the probability of a clutch producing a hatchling and the probability of a clutch producing a fledgling Hatching Fledging Predicted probabilities C1 C2 Reduced Enlarged C1 C2 Reduced Enlarged Early lay period Late lay period 0.68 0.27 0.86 0.53 0.65 0.64 0.89 0.50 0.41 0.16 0.77 0.47 0.62 0.31 0.69 0.37 Early lay period Late lay period Across lay periods Comparisons t240 p-value di t75 p-value t314 p-value di Reduced versus C2 Enlarged versus C1 Enlarged versus reduced C2 versus C1 Enlarged versus C2 Reduced versus C1 3.17 2.15 2.75 2.17 0.51 0.28 .0021 .0324 .0062 .0313 .6135 .7826 0.008 0.033 0.017 0.025 0.042 0.050 0.63 1.06 0.63 1.50 0.18 1.67 .528 .293 .532 .137 .860 .099 2.23 2.48 0.74 3.85 1.25 1.93 0.0273 0.0142 0.4576 ⬍0.0011 0.2125 0.0554 0.025 0.017 0.050 0.008 0.042 0.033 p-value, achieved significance level; di, critical significance level from false discovery rate procedure. After arranging comparisons in order of decreasing p-values, if p-value ⬍ di then the null hypothesis for that comparison and for all remaining comparisons are rejected. Superscripts on p-values indicate ordering. One marginally significant and all significant comparisons appear in bold. 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 Achick 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 Figure 1 Proportion of clutches in each treatment group that produced at least one hatchling, classified by lay period. Bars represent the 95% confidence interval for proportions, and sample sizes are in parentheses. 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. 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. 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 344 Figure 2 Proportion of clutches in each treatment group that produced a fledgling, classified by lay period. Bars represent 95% confidence intervals, and sample sizes are in parentheses. the 1% down stage across treatment groups (ANCOVA, F3, 192 ⫽ 0.83, p ⫽ 0.48). DISCUSSION 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. Behavioral Ecology Vol. 12 No. 3 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. Clifford and Anderson • Insurance eggs in boobies 345 Table 3 Observed hatching success (HS) for C2 and enlarged clutches, as well as the observed and expected numbers and proportions of clutches that produced two, one, or zero hatchlings Number of clutches (proportion) that produced Treatment HS C2 0.638 Enlarged 0.596 Observed Expected Observed Expected Two chicks One chick Zero chicks 85 68 21 20 43 77 26 27 39 22 10 9 (0.509) (0.407) (0.368) (0.355) (0.257) (0.462) (0.456) (0.482) (0.234)* (0.131)* (0.175) (0.163) HS, number of eggs that hatched/number of eggs laid. Expected proportions are calculated from observed hatching success for each group (e.g., expected proportion of C2 clutches to produce two chicks ⫽ (0.638)(0.638) ⫽ 0.407). * 2 ⫽ 32.4, df ⫽ 2, p ⬍ .001. 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 probablity 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 pro- portion 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. 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, rockhopper 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 indi- 346 viduals 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). 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