Experimental demonstration of the insurance value of extra eggs in an obligately siblicidal seabird

A variety of organisms regularly produce more offspring thanthey raise. Despite the apparent energetic waste of such areproductive tactic, overproduction may be favored by naturalselection in some cases. One such case is when surplus offspringcan serve as replacements, or insurance, for failed siblings.We tested the Insurance Egg Hypothesis (IEH) as an explanationfor the overproduction of offspring in an obligately siblicidal seabird, the Nazca booby (Sula grant)i, which fledges a maximumof one nestling regardless of its clutch size. We manipulatedclutch sizes within the range of natural variation encounteredin this species (one-two eggs). The IEH predicts that parentswith two-egg clutches should have higher reproductive successthan those with one-egg clutches because the second egg canprovide a nestling when the first egg fails to hatch, or when the first chick dies young. Consistent with the IEH, naturalone-egg clutches that were enlarged to two eggs produced morehatchlings and fledglings than control one-egg clutches did,and natural two-egg clutches that were reduced to one egg producedfewer hatchlings and fledglings than control two-egg clutchesdid. We also evaluated aspects of the Individual Optimization Hypothesis, which proposes that individual optimal clutch sizesdiffer, as an explanation for clutch size variation in thisspecies. In Nazca boobies, selection driven by replacementvalue appears to favor clutches larger than one even thoughfinal brood size is invariably one. One-egg clutches may be produced by parents experiencing some proximate limitation,such as a lack of food.     

Paternal care and male mate-attraction effort in the European starling is adjusted to clutch size

In facultative polygynous birds with biparental care, a trade-off may occur between male parental care and attraction of additional mates. If there is a cost associated with reduced male parental care, the relative benefit of mate attraction may be predicted to decrease as the size of a male's clutch or brood increases. We tested this prediction in monogamous pairs of facultatively polygynous European starlings (Sturnus vulgaris). The larger the clutch, the more time the male spent incubating and the less time he spent attracting an additional female (i.e. singing near and carrying green nesting material into adjacent empty nest-boxes). Reduced paternal incubation resulted in lower overall incubation (the female did not compensate) and lower hatching success. Immediately after experimental reduction of clutches, males spent significantly less time incubating and more time singing and carrying greenery, and vice versa for experimentally enlarged clutches. Males with experimentally reduced clutches attracted a second female more often than males with experimentally enlarged clutches. This is the first study, to our knowledge, to provide experimental evidence for an adjustment of paternal care and male mate-attraction effort to clutch size. However, a trade-off between paternal nestling provisioning and mate attraction was not revealed, probably due to the absence of unpaired females by that time in the breeding season. Experiments showed that the relative contribution of the male and female to nestling provisioning was unrelated to brood size.     

Offspring fitness and individual optimization of clutch size

Within-year variation in clutch size has been claimed to be an adaptation to variation in the individual capacity to raise offspring. We tested this hypothesis by manipulating brood size to one common size, and predicted that if clutch size is individually optimized, then birds with originally large clutches have a higher fitness than birds with originally small clutches. No evidence was found that fitness was related to the original clutch size, and in this population clutch size is thus not related to the parental capacity to raise offspring. However, offspring from larger original clutches recruited better than their nest mates that came from smaller original clutches. This suggests that early maternal or genetic variation in viability is related to clutch size.     

Are incubation costs in female pied flycatchers expressed in humoral immune responsiveness or breeding success?

Although clutch size variation has been a key target for studies of avian life history theory, most empirical work has only focused on the ability of parents to raise their altricial young. In this study, we test the hypothesis that costs incurred during incubation may be an additional factor constraining clutch size in altricial birds. In the pied flycatcher (Ficedula hypoleuca), we manipulated the incubation effort of the female by enlarging and reducing clutch sizes. To manipulate incubation effort only, the original clutch sizes were restored shortly after hatching. We found that fledging success was lower among broods whose clutches were enlarged during incubation. There was, however, no effect of manipulation on female body condition or on their ability to mount a humoral immune response to diphtheria or tetanus toxoid during the incubation or nestling provisioning period. Instead, we found that the original clutch size was related to the immune response so that females with seven eggs had significantly lower primary antibody responses against tetanus compared to those with six eggs. Our results suggest that incubating females are not willing to jeopardise their own condition and immune function, but instead pay the costs of incubating a larger clutch by lower offspring production. The results support the view that costs of producing and incubating eggs may be substantial and hence that these costs are likely to contribute to shaping the optimal clutch size in altricial birds.     

Resource-Dependent Clutch Size Decisions and Size-Fitness Relationships in a Gregarious Ectoparasitoid Wasp, <Emphasis Type="Italic">Bracon brevicornis</Emphasis>

Gregarious parasitic wasps, which lay more than one egg into or onto a host arthropod’s body, are usually assumed to lay an optimal number of eggs per host. If females would lay too few eggs, some resources may be wasted, but if females lay too many eggs, offspring may develop into substantially smaller-sized adults or may not develop successfully and die. The availability of hosts can further influence a female’s clutch size decision, as more eggs should be laid when hosts are scarce. Here, we analyzed clutch size decisions and the fitness consequences thereof in the ectoparasitic wasp Bracon brevicornis (Hymenoptera: Braconidae), a potential biocontrol agent against pest moth species. For experiments, larvae of the Mediterranean flower moth, Ephestia kuehniella (Lepidoptera: Pyralidae) were used. Using artificially created as well as naturally laid clutches of eggs, the effects of clutch size on fitness of first (F1) and second (F2) generation offspring were investigated. Our results revealed that the fitness consequences of large clutches included both increased mortality and smaller adult sizes of the emerging offspring (F1). Smaller F1 females matured fewer eggs during their lifetime and their offspring (F2) had reduced egg-to-adult survival probability. Naturally laid clutches varied with host size up to a maximum, which probably reflects egg limitation. Clutches remained smaller than the calculated optimal (Lack) clutch size and females responded to high host availability with a decreased number of eggs laid. We thus conclude that large clutches may result in significantly smaller offspring with reduced fitness, and that host size as well as host availability influence the clutch size decision made by B. brevicornis females.     

More colourful eggs induce a higher relative paternal investment in the pied flycatcher Ficedula hypoleuca: a cross-fostering experiment

The signalling hypothesis of eggshell colouration in birds posits that females of species with blue-green eggs signal their phenotypic quality or the quality of their eggs to their mates through deposition of the antioxidant biliverdin as pigment. Males respond by investing more in the offspring. Through a cross-fostering experiment where we have exchanged whole clutches between pairs of pied flycatcher Ficedula hypoleuca nests, we managed to break potential associations between female quality and clutch chromaticity. We show that males respond to incubated clutches with more variable and higher peak values in blue-green chroma through a higher proportional investment in nestling provisioning on day 4 of the nestling period, when males invest more heavily than females in provisioning. More variable clutches show higher peak chroma values. We also show that egg colour during the two-week incubation period has a significant effect, which is not found for the colour of eggs during the laying period. Finally, the proportion of male provisioning visits affects negatively female brooding effort and nestling mortality, and thereby has positive effects on female fitness. Blue-green chroma in the pied flycatcher functions as a signal of female or clutch quality to males which respond by adjusting their relative investment with respect to total pair effort.     

Inter-sexual differences in the immune response of Eurasian kestrel nestlings under food shortage

When resources are limited, parents should decide the optimal number, size, and sex of progeny, and offspring should decide the optimal allocation of resources to different costly functions, such as growth and immunity. We manipulated clutch sizes of Eurasian kestrels by one egg to estimate possible cumulative effects of incubation and chick rearing costs on parental body condition, feeding effort, and offspring viability. No obvious effects of clutch size manipulations on feeding effort were found while feeding effort was adjusted to the original clutch size. Enlarged and control nests suffered from higher nestling mortality than reduced nests, and chicks of the enlarged group were in poorer body condition than chicks of the reduced group. Controlling for body mass, male chicks exhibited lower cell-mediated immunity assessed by a cutaneous hypersensitivity response than females, but only in treatments suffering from food restrictions, as indicated by chick starvation. These novel results reveal inter-sexual differences in physiological strategies in early life, suggesting sex-related differences in susceptibility to disease and consequently in survival prospects of offspring.     

Nest size affects clutch size and the start of incubation in magpies: an experimental study

Nest size has been suggested to be a sexually selected traitindicating parental ability of both males and females. To testwhether a female's reproductive decisions (e.g., clutch sizeand starting incubation) change in relation to experimentalmanipulation of nest size, as would be predicted if nest sizeis a sexually selected signal reflecting the male's parental quality, we manipulated nest size in a population of monogamousmagpies before laying by adding or removing about 20 cm oflarge sticks in the roof of magpie nests. On the one hand,we found that clutch size of reduced nests was smaller thanthat of control or enlarged nests. Moreover, clutch size was significantly related to nest size after manipulation, whichindicates that females adjust clutch size to the final sizeof the nest, nest size thereby being a good candidate for asexually selected trait. On the other hand, number of eggshatched during the first day is hypothesized to be related to the expected available resources during nestling growth, andsubsequent nestlings hatched are likely to die due to broodreduction if resources are not sufficient to raise well-developednestlings. Nest size is hypothesized to inform females abouta male's willingness to invest in reproduction, and we foundthat in broods of experimentally reduced nests, females startedto incubate earlier in the laying sequence than they did inbroods of control or enlarged nests. Moreover, in experimentallyreduced nests, fewer nestlings hatched during the first day,and the difference in body mass between the first and the fourthnestling hatched increased. This result is in accordance withthe hypothesis that the female's decision of when to start incubationin the laying sequence is mediated by nest size, a sexuallyselected trait signaling parental quality. We discuss alternativeexplanations for the results such as the possibility that nestsof different treatments may differ in their thermoregulationproperties or in their protection against predators.     

Clutch size and the costs of incubation in the house wren

Trade-offs in the allocation of finite resources among differentstages of a breeding attempt as well as between different reproductiveevents should shape the evolution of life-history traits. Toinvestigate the effects of incubation effort on within-broodand between-brood trade-offs in house wrens (Troglodytes aedon),we manipulated the clutch size that females incubated. We isolatedeffects of incubation by reversing the manipulation at hatchingto allow all parents to provision their natural brood sizes.Females that incubated enlarged clutches had longer incubationperiods than control females, both early and late in the season,suggesting that the experimental treatment increased incubationeffort. Contrary to predictions, however, increased incubationeffort did not adversely affect the allocation of effort tonestling provisioning. Rather, in the early season, but notin the late season, females that incubated enlarged clutchesappeared to allocate more effort to nestling provisioning, producingheavier and larger fledglings than control females. Althoughfemales with enlarged early-season clutches consequently lostmore mass than control females, this was likely an adaptiveresponse to reduce wing loading in anticipation of high provisioningdemands. There were no treatment-related differences in fledglingmass or size, or in female mass loss, in the late season. Thus,elevated incubation demands negatively affected a fitness-relatedtrait (duration of incubation) that may constrain clutch sizebut not the allocation of resources to subsequent stages ofthe same breeding event or to subsequent breeding events. Wesuggest that environmental conditions may mediate clutch-sizeeffects on trade-offs in allocation of resources between incubationand nestling provisioning.     

Clutch size manipulation, hatching success and offspring phenotype in the ball python (Python regius)

In a diverse array of avian and mammalian species, experimental manipulations of clutch size have tested the hypothesis that natural selection should adjust numbers of neonates produced so as to maximize the number of viable offspring at the end of the period of parental care. Reptiles have not been studied in this respect, probably because they rarely display parental care. However, females of all python species brood their eggs until hatching, but they do not care for their neonates. This feature provides a straightforward way to experimentally increase or reduce clutch size to see whether the mean clutch size observed in nature does indeed maximize hatching success and/or optimize offspring phenotypes. Eggs were removed or added to newly laid clutches of Ball Pythons ( Python regius ) in tropical Africa (nine control clutches, eight with 50% more eggs added, six with 42% of eggs removed). All clutches were brooded by females throughout the 2-month incubation period. Experimental manipulation of clutch-size did not significantly affect the phenotypes (morphology, locomotor ability) of hatchlings, but eggs in 'enlarged' clutches hatched later, and embryos were more likely to die before hatching. This mortality was due to desiccation of the eggs, with females being unable to cover 'enlarged' clutches sufficiently to retard water loss. Our results support the notion of an optimal clutch size, driven by limitations on parental ability to care for the offspring. However, the proximate mechanisms that generate this optimum value differ from those previously described in other kinds of animals. © 2003 The Linnean Society of London . Biological Journal of the Linnean Society 2003, 78 , 263–272.     

Encountering competitors reduces clutch size and increases offspring size in a parasitoid with female-female fighting

Understanding the size of clutches produced by only one parent may require a game-theoretic approach: clutch size may affect offspring fitness in terms of future competitive ability. If larger clutches generate smaller offspring and larger adults are more successful in acquiring and retaining resources, clutch size optima should be reduced when the probability of future competitive encounters is higher. We test this using Goniozus nephantidis, a gregarious parasitoid wasp in which the assumption of size-dependent resource acquisition is met via female-female contests for hosts. As predicted, smaller clutches are produced by mothers experiencing competition, due to fewer eggs being matured and to a reduced proportion of matured eggs being laid. As assumed, smaller clutches generate fewer but larger offspring. We believe this is the first direct evidence for pre-ovipositional and game-theoretic clutch size adjustment in response to an intergenerational fitness effect when clutches are produced by a single individual.     

Intraseasonal effects of clutch manipulation on parental provisioning and residual reproductive value of eastern phoebes (Sayornis phoebe)

Summary First clutches of double-brooded eastern phoebes Sayornis phoebe were manipulated (up two eggs, down 2 eggs or no change) to test for intraseasonal reproductive tradeoffs and to test whether size of first brood influenced food delivery rates to nestlings and nestling quality in second broods.Considering all nests from both broods, rate of feeding nestlings increased linearly with brood size but nestling mass per nest decreased with increasing brood size. High nestling weights in small broods may have resulted from parents delivering better quality food, but we did not test this.Among treatment groups in first broods, nestlings from decreased broods weighed more than those in control or increased broods. Treatment did not influence the likelihood that second nests would be attempted after successful first nests nor did it alter the interval between nests. Nestlings of parents that renested weighed more than those of parents that did not, regardless of treatment, suggesting that post-fledging care may preclude renesting. Mass of individual females did not change between broods, regardless of brood size. Clutch sizes of second attempts were not affected by manipulations of first broods but increasing first broods reduced the number of nestlings parents were able to raise to day 11 in their second broods. However, manipulation of first broods did not affect mean nestling mass per nest of nestlings that survived to day 11.In phoebes, parents of small first broods are able to raise nestlings in better condition. We predict that in harsh years, parents of small first broods would be more likely to renest. Parents of enlarged first broods sacrificed quality of offspring in second broods, which seems a reasonable strategy if nestlings from second broods have lower reproductive value.     

Clutch size relative to tree cavity size in Northern Flickers

We analysed clutch size versus nest size in 153 broods of the Northern Flicker Colaptes auratus , a woodpecker using natural cavities in British Columbia, Canada. Larger volume cavities were less susceptible to predation and cavity size was positively associated with the age and body size of males and with the body condition of female parents. Although clutches varied between 4 and 11 eggs, and the floor area of cavities varied about 5-fold, we found no relationship between clutch size and floor area or cavity volume. To see if there were fitness consequences to clutch size relative to nest size, we examined hatching success and nestling mortality in flicker broods. Hatching success was not related to cavity size, but crowding slightly reduced nestling survival even when clutch size was controlled statistically. However, there was no effect of cavity size on the total number of nestlings fledged. Newly excavated flicker cavities were smaller than reused cavities suggesting a cost to excavation. This cost, coupled with the minimal fitness consequences of overcrowding, may explain why flickers do not adjust clutch size to cavity size.     

Eggshell pigmentation pattern in relation to breeding performance of blue tits Cyanistes caeruleus

1. We test the consequences, in terms of breeding success and parental effort, of eggshell pigmentation pattern in a hole-nesting bird, the blue tit Cyanistes caeruleus that lays eggs asymmetrically speckled with reddish spots (maculated eggs). 2. We assess the effect of distribution of spots (pigment 'spread') and spot size and pigment intensity (pigment 'darkness') on eggshell physical properties and breeding parameters concerning nestling condition, investment of parents in offspring care and reproductive output in two different habitat types: a deciduous oakwoodland and an evergreen forest. 3. Blue tit clutches with more widely distributed spots showed a thicker eggshell, a shorter incubation period, a lesser amount of mass loss per day and a higher hatching probability than those with spots forming a 'corona' ring. While eggs with larger and darker (more pigment intensity) spots showed a thicker eggshell and a shorter incubation period. In the light of 'signal function hypothesis', these egg traits may reflect female health status and, consequently, this could affect male parental effort. 4. Here we show supports for some of the necessary assumptions of this hypothesis. We found a positive relationship between egg pigment 'spread' and male but not female provisioning rates per day. On the other hand, pigment 'darkness' of blue tits' clutches was positively related to female tarsus length, while pigment 'spread' was positively related to clutch size, male body mass and nestling tarsus length. Our study shows that eggshell pigment 'spread' can be used as an indicator of clutch quality. Further investigations are needed to understand the role of calcium availability as possible causal agent of deviant eggs and its relation to the maculation phenomenon.     

Proximate causes and fitness consequences of hatching failure in lesser kestrels Falco naumanni

Hatching failure is a pervasive phenomenon in birds, but factors affecting hatchability remain poorly understood. We studied proximate causes and fitness consequences of hatching failure in a long‐monitored population of the colonial lesser kestrel Falco naumanni. We investigated whether hatchability was related to clutch characteristics, parental traits, and social or environmental features. Hatching failure represents a cost for the parents in terms of immediate fitness, since it reduced both their number of young fledged and recruits in the breeding population, even when controlling for clutch size. Hatching failure showed a non‐linear relationship with clutch size, clutches of four eggs showing higher levels of hatching success than larger or smaller clutches. Hatchability could therefore play a role in the evolution of optimal clutch size in this species, at least constraining the maximum number of eggs the parents can afford to incubate. Contrary to most studies, the mean volume of the clutch and the individual egg volume were negatively related to hatching failure, indicating that large eggs have thermoregulatory and/or nutritional advantages. Mean daily maximum temperature during incubation affected hatching success negatively, but only for females in poor condition. This result seems to indicate that females are reluctant to jeopardize their own condition, but instead sacrifice incubation effort by paying the costs of a lower hatching success in circumstances of high temperatures. There was no evidence that hatching failure was related to the intrinsic properties of individuals or genetic similarity between the parents as indicated by low repeatabilities of: (1) males that bred with different females, (2) females that bred with different males, and (3) pairs breeding together in different years. Neither colony size nor subpopulation size affected hatchability. All these findings show how hatching failure is simultaneously influenced by several factors acting in a complex way, which could in part explain the apparently conflicting conclusions of empirical or even experimental studies carried out to date.     

Selection for synchronous breeding in the European starling

Colonial birds often demonstrate considerable breeding synchrony. In southern Sweden the semi-colonial European starling initiated the vast majority of clutches within one week. Laying dates were positively skewed so that many birds initiated clutches at similar dates early in the season. Breeding was further synchronised by a particularly strong clutch-size reduction equivalent to one third of an egg per day during the first part of the breeding season. The decline in clutch size with season also held true for separate age-classes of females, for individual females laying at different times at different years and for individual females laying at different times the same year. Trends in breeding success during nestling rearing were unlikely to explain the high degree of breeding synchrony or the seasonal decline in clutch size; nestling survival and growth were weakly related or unrelated to reproductive timing. In contrast recruitment success of fledged offspring declined sharply with season. Even within the synchronous laying period, defined as clutches initiated during the first week each year, local recruitment success declined. It is suggested that the early seasonal decline is caused by selection for synchronous fledging permitting the immediate formation of flocks after fledging, whereas the late seasonal trends may be caused by either population differences in female quality or deteriorating conditions for raising young.     

The trade-off between molt and parental care: a sexual conflict in the blue tit?

Breeding activities and molt are generally thought to be mutuallyexclusive in birds since both are energetically costly and arenormally separated in time. However, sometimes molt overlapswith breeding to some degree. A trade-off between adult somaticmaintenance functions (feather renewal) and parental care isthen to be expected. The consequences of this are largely unknown,and there are few studies that have shown any fitness costsof molt-breeding overlap. We investigated the consequences ofmolt-breeding overlap by removing first clutches of blue titParus casruleus pairs, thereby inducing late repeat clutches.Among the delayed pairs, a high proportion of males and somefemales started their molt already during incubation or nestlingfeeding. Molting males fed their nestlings to a lesser extentthan non-molting ones, and nestling mortality increased as adirect result of the early timing of male molt. Furthermore,the ability to raise an experimentally enlarged brood was negativelycoupled to the molt stage of the male. Our data thus provideevidence that molt-breeding overlap leads to fitness costs,and we discuss the results within the context of sexual conflictand the implications for optimization of avian reproductivedecisions     

Nestlings’ carotenoid feather ornament affects parental allocation strategy and reduces maternal survival

In some birds, feather ornaments are expressed in nestlings well before sexual maturation, possibly in response to parental favouritism towards high‐quality offspring. In species with synchronous hatching, in which nestling ornaments may vary more among than within broods, parents may use this information to adjust their parental allocation to the current brood accordingly. We tested this hypothesis in the rock sparrow, in which a sexually selected yellow feather ornament is also expressed in nestlings. We experimentally enlarged nestlings’ breast patch in a group of broods and sham‐manipulated another group of control broods. Nestlings with enlarged ornament were fed more frequently and defended more actively from a dummy predator than their control counterparts. Mothers from the enlarged group were more likely to lay a second clutch and showed a reduced survival to the next breeding season. These results provide one of the first evidences of differential parental allocation among different broods based directly on nestlings’ ornamentation, and the first, to our knowledge, to show a reduction in maternal survival.     

Clutch size manipulations in two seed beetles: consequences for progeny fitness

Seed beetles (Coleoptera: Bruchidae) lay their eggs on discrete resource patches, such that competition among larvae for food is an important component of their biology. Most seed beetles, including Stator limbatus, lay eggs singly on individual seeds and avoid superparasitism except when seeds are limiting. In contrast, S. beali, a closely related congener, lays eggs in clutches on a single seed. We tested the hypothesis that natural selection on larval life history characters favors small clutches (selection against large clutches) in S. limbatus, but that selection against large clutches is relaxed in S. beali because of the large size of its host's seeds. We manipulated clutch size and examined its relationship to offspring fitness. Clutch size affected the survivorship of S. limbatus larvae(r ²=0.14), but had no detectable effect on the survivorship of S. beali larvae (r ²=0.04). Also, clutch size had a large effect on development time and body weight of S. limbatus, but not of S. beali. We discuss the implications of this result for the evolution of clutch size in S. limbatus and S. beali.     

The significance of clutch overlap in Great Tits Parus major

We studied the effects of manipulation of the size of first broods in the Great Tit Parus major on the size and breeding success of second clutches and its relation to the degree of clutch overlap. The rearing of first brood fledglings always overlapped with the laying of the second clutch and in most cases also with the incubation period of the latter. The degree of clutch overlap depended on the size of the first brood, being less when the first brood was large. Clutch overlap also increased with season. Mechanisms affecting the timing of laying of second clutches are discussed. A large first brood imposed reproductive costs. It affected the size of the second clutch by causing it to be delayed; second clutch size decreases with season. It affected the post-fledging survival of second brood young as, in this population, this decreases with fledging date. The breeding success of second clutches was, however, not affected by the size of the first brood, but instead by the weight of the female when rearing the first brood.