Eggshell structure, mode of development and growth rate in birds

The shell of an egg contributes to successful embryogenesis in many ways, such as through protection, respiration and water exchange. The shell is also the major source of calcium for the development of high-calcium consuming organs, e.g. the skeleton, muscles and brain. Some studies show, moreover, that growth rate may play a fundamental role in the pattern of skeletal development in birds: the faster the growth the less ossified the skeleton is at hatching. We predicted, therefore, that slow (precocial) and fast (altricial) growing bird species should lay eggs encased in shells with different structures adapted to support different rates of calcium removal by developing embryos. We tested this prediction by comparing the fine structure of the inner eggshell surface (mammillary layer) from 36 bird species belonging to 18 orders ranging from Struthioniformes to Passeriformes. Using scanning electron microscopy, we compared the mammillary layer of both non-incubated eggs and eggs at the time of hatching, i.e., before and after embryonic development and the accompanying calcium removal. The results were consistent with the prediction, i.e., the number of mammillary tips per unit of surface area was associated with mode of development and growth rate. The number was higher, and calcium removal was also more extensive, in shells from precocial bird species than in shells from altricial bird species.     

Evolution of avian eggshell structure

Data are presented suggesting that birds have evolved eggs with shells containing different structures (numbers of mammillae per unit of inner eggshell surface area, i.e., mammillary densities) to cope up with different calcium requirements imposed by different growth rates and modes of development. Precocial bird species grow slowly, but have high mammillary density, while altricial bird species grow rapidly, but have low mammillary density. These results suggest an adaptation associated with growth rate and mode of development and show, moreover, that the mammillary layer is indicative of the breeding biology of the bird. J. Morphol. 2012. © 2011 Wiley Periodicals, Inc.     

How to hatch from an egg of great structural strength. A study of the Common Cuckoo

Brood parasitism represents a unique mode of avian reproduction that requires a number of adaptations. For example, to reduce chances of puncture ejection of their eggs by small hosts, brood parasites may have been selected for laying eggs of unusually great structural strength. However, great structural strength of eggshells should hinder hatching. The goals of our study were to establish if chicks of the Common Cuckoo Cuculus canorus have more difficulty with hatching out of their strong eggs than chicks of species with eggs of similar size, and whether they possess any mechanisms facilitating hatching. To achieve these goals, we compared hatching pattern and selected body characteristics of chicks of the Common Cuckoo with those of another altricial species with eggs of a similar size, the Great Reed Warbler Acrocephalus arundinaceus . Although the rate of pecking was similar in the two species, the Common Cuckoo chicks started pecking earlier in relation to their emergence and consequently required more time and a greater cumulative number of pecks for breaking open their eggs than did young Great Reed Warblers. The two species also differed with respect to the pattern of opening their shells; in contrast to the warbler chicks, which enlarged the original pip circularly, the cuckoo chicks opened the egg by systematically creating a long narrow slit until they emerged. Finally, our study of hatched young revealed several differences; the Cuckoo hatchlings were significantly heavier, had a longer forearm, and their egg tooth was located significantly farther from the tip of the beak. The edge used for cutting through the shell was also significantly longer than that of hatchling Great Reed Warblers. To conclude, our data suggest that hatching is more difficult for a Cuckoo than for a Great Reed Warbler and that Cuckoos possess several mechanisms to overcome the problems of hatching from a structurally strong egg.     

The evolution of obligate interspecific brood parasitism in birds

We present a simple analytical model to investigate the conditionsfor the evolution of obligate interspecific brood parasitismin birds, based on clutch size optimization, when birds canlay more eggs than their optimal clutch size. The results showthat once intraspecific parasitism has appeared (i.e., femalesstart to spread their eggs over their own and other nests) the evolutionarily stable number of eggs laid in its own nest decreases.Two possible ESSs exist: (1) either the evolutionarily stablenumber of eggs laid in its own nest is larger than zero, anda fraction of the total number of eggs is laid parasitically(i.e., intraspecific parasitism); and (2) either the evolutionarilystable number of eggs laid in its own nest is zero and all eggs are laid parasitically. Since all females lay parasitically,this could favor the evolution of obligate interspecific broodparasitism. The key parameter allowing the shift from intraspecificto obligate interspecific parasitism is the intensity of density-dependentmortality within broods (i.e., nestling competition). Strongnestling competition, as in altricial species, can lead toan ESS where all eggs are laid parasitically. Altricial speciesare, therefore, predicted to evolve more easily toward obligate interspecific parasitism than precocial species. These predictionsfit the observed distribution of brood parasitism in birds,where only one species out of 95 obligate interspecific parasitesexhibits a precocial mode of development. Different nestlingsurvival functions provided similar findings (i.e., obligatebrood parasitism is more likely to evolve in altricial species),suggesting that these results are robust with respect to themain assumption of the model.     

Life-history styles of fishes in South African estuaries

Synopsis Fish utilizing South African estuaries may be divided into two major groups according to the location of their spawning sites. The marine group comprises large species which spawn at sea, enter estuaries mainly as juveniles, and return to the sea prior to attaining sexual maturity. The estuarine group is dominated by small species which have the ability to complete their life cycle within the estuarine environment. They tend to produce relatively few, demersal eggs, or exhibit parental care, which facilitates the retention of eggs and young within the estuary, whereas the marine group release large numbers of small pelagic eggs during spawning and exhibit no parental care. This is contrary to the theory that estuaries (unpredictable environments) should favour altricial life-history styles and the marine inshore zone (a more predictable environment) should favour precocial styles. However, if the total ichthyofauna of South African estuaries is considered, then altricial species predominate. The fact that both altricial and precocial traits are well represented within the overall estuarine fish community suggests that the various taxa have adapted their life-history styles, in different ways, to ensure the utilization of abundant food resources available within these fluctuating systems. A detailed comparison of the life-history styles of the estuarine teleostGilchristella aestuaria and the marine fishMugil cephalus is used to illustrate the contrasting manner in which these two species have succeeded in exploiting South African estuaries.     

Effects of egg size on Double-crested Cormorant (Phalacrocorax auritus) egg composition and hatchling phenotype

Maternal investment of yolk and albumen in avian eggs varies with egg mass and contributes to variation in hatchling mass. Here we use the natural variation in mass and composition of Double-crested Cormorant (Phalacrocorax auritus) eggs to examine consequences of variation in yolk and albumen mass on hatchling phenotype. The Double-crested Cormorant, a large bird with altricial young, lays eggs ranging in mass from 40 to 60 g and containing an average of 82% albumen and 18% yolk. Variation in Cormorant egg mass arises primarily from variation in the amount of albumen and water in the eggs; yolk mass remains relatively constant, contributing only 10% to egg mass variation. Likewise, variation in hatchling mass correlates positively with albumen mass and albumen solids contribute to hatchling dry mass. Thus, variation in Cormorant egg mass is primarily the result of variation in the amount of egg albumen, which contributes most to variation in hatchling mass. Similarities in egg composition of altricial birds, along with data presented here, suggest that variation in hatchling mass of all altricial birds may depend most on the amount of egg albumen, unlike species with precocial young that hatch from eggs with substantially more yolk.     

Mode of development and interspecific avian brood parasitism

Avian interspecific brood parasites differ considerably in theircommitment to parasitism; 87 species are obligate brood parasites,whereas 35 species are known to be facultative brood parasites.This variation is strongly related to mode of development. Obligateparasitism is found almost exclusively in altricial species,whereas facultative interspecific parasitism is predominantin precocial birds. We propose that the association betweenmode of development and form of parasitism reflects a fundamentaldifference between altricial and precocial birds in the relativebenefits of emancipation from parental care after laying. Weargue that altricial brood parasites obtain such a large increasein realized fecundity by avoiding the costs of parental carethat obligate parasitism is favored over facultative parasitism.In contrast, precocial brood parasites gain relatively littlein terms of increased fecundity via obligate parasitism, andmuch of this increase could potentially be gained by facultativeparasitism. Thus, obligate interspecific brood parasitism willnot be favored in precocial birds. Three factors influence thisdifference between altricial and precocial species: (1) altricialbirds have relatively more energy and nutrients with which tolay additional eggs, (2) altricial birds can produce more eggsfor the same amount of energy and nutrients, and (3) altricialbirds realize a greater relative gain in fecundity for eachadditional egg laid. We suggest further that facultative interspecificparasitism in birds may originate simply through a carry overof intraspecific parasitism; 29 of 33 facultative interspecificparasites also parasitize conspecifics. Facultative parasitismof other species would provide a greater range of potentialhost nests and could be maintained as an evolutionarily stableend point by the same mechanisms that maintain intraspecificbrood parasitism. [Behav Ecol 1991;2:309–318]     

Water in the Avian Egg Overall Budget of Incubation

The loss of mass in eggs during incubation was examined andevidence is presented to show that this is essentially due toloss of water. The mean fraction of water lost by diffusionthroughout incubation is 0.150 ± 0.025 S D per gram ofegg and 0.162 ± 0.026 S D per gram of egg content for81 species. The water fraction of fresh eggs and of hatchingeggs was examined in 32 species divided according to maturityat hatching, and found to be very similar within each category(83% in altricial 83% in semi-altricial 78% in semi-precocial72% in precocial eggs). The 11% difference between the altricialand precocial categories is statistically significant. Duringincubation, dry matter is metabolized increasing the water fractionwhich is further increased by metabolic water production. Hence,water loss during incubation is mandatory if the relative watercontent of an egg at the end of incubation is to remain essentiallythe same as at the beginning. Equations are developed whichallow one to estimate the difference between diffusive waterloss and the total water loss in altricial and piecocial eggscaused by additional water loss during pipping and hatching.     

Egg shape and size allometry in geckos (Squamata: Gekkota), lizards with contrasting eggshell structure: why lay spherical eggs?

Hard, highly calcified eggshells evolved several independent times during the history of amniotes. Because of phylogenetic conservatism of this trait, lineages in which closely related taxa differ in eggshell structure are rare. Four gekkotan families (Carphodactylidae, Diplodactylidae, Eublepharidae and Pygopodidae) have eggs with soft shells, while their close relatives (Gekkonidae) lay eggs with hard shells. Geckos thus offer a rare opportunity to compare the impact of the emergence of a hard eggshell on the economy of egg architecture. Because a sphere has the smallest surface area of all three‐dimensional solids of a given volume, spherical eggs in geckos with hard eggshells reduce calcium investment and should therefore be advantageous. Here, we document that hard‐shelled gekkonid eggs are indeed more spherical than those of the other gecko lineages. However, within gekkonids, small species lay more elongated eggs than larger species. We speculate that miniature gekkonid females, which lay larger eggs relative to body size compared with large gekkonids, produce elongate eggs in order to pass the egg through a limited pelvic opening.     

Basal hatching by Maculinea butterfly eggs: a consequence of advanced myrmecophily?

Larvae of Maculinea alcon and M. rebeli are unique among Holarctic Lycaenidae in hatching through the base of the eggshell and emerging on the opposite side of the leaf to the egg. This occurs because the exposed upper surfaces of their eggs have exceptionally thick shells. Other species of Maculinea have normal or unusually thin-shelled eggs. It is suggested that both types of Maculinea eggshell have evolved to reduce mortalities from parasitoids and predators. Maculinea alcon and M. rebeli are forced to lay in exposed places due to the structure of their foodplants, and protect their eggs with thick shells. The other three species hide their eggs deep within the inflorescences of their foodplants; M. nausithous and M. teleius require thin flexible shells to achieve this. These adaptations are necessary because Maculinea eggs often occur at much higher densities on their initial foodplants and are hence more vulnerable—than is the case with other Lycaenidae. This is a consequence of myrmecophily. Maculinea population size is regulated more by the status of the ant host than by that of the initial foodplant. Large Maculinea populations, and high densities of eggs, occur on the many sites where the ant is abundant but the foodplant is scarce. Maculinea alcon and M. rebeli eggs occur at the highest densities, and need the greatest protection, due to the advanced form of myrmecophily found in these species. Whereas M. anon, M. teleius and M. nausithous larvae are predators of ant brood, M. alcon and M. rebeli feed mainly at a lower trophic level on ant regurgitations. This leads to roughly seven times more M. alcon and M. rebeli adults emerging per ant nest, and to a similar increase in egg densities per foodplant.     

Competing Females and Caring Males. Polyandry and Sex-Role Reversal in African Black Coucals, Centropus grillii

Most species of birds show bi‐parental or female‐only care. However, a minority of species is polyandrous and expresses male‐only care. So far, such reversals in sex roles have been demonstrated only in precocial bird species, but there was suggestive evidence that such a mating system may occur in one altricial bird species, the black coucal, Centropus grillii. In a field study in Tanzania we investigated whether black coucals are sex‐role reversed and polyandrous. We found that males were mated to one female, rarely vocalized and provided all parental care from incubation of eggs to feeding of young. In contrast, female black coucals were about 69% heavier and 39% larger than males and polyandrous. They spent a large proportion of time calling from conspicuous perches, defended breeding territories, did not help in provisioning young and had a higher potential reproductive rate than males. We conclude that the black coucal currently represents the only altricial bird species with sole male parental care and a classical polyandrous mating system. High nest predation pressure and small territory sizes due to high food abundance may have been important factors in the evolution of sex‐role reversal and polyandry in this species.     

Evolutionary lag versus bill-size constraints: a comparative study of the acceptance of cowbird eggs by old hosts

Summary Evolutionary lag and resistance to puncture-ejection are two hypotheses explaining why hosts long exposed to brood parasitism by molothrine cowbirds accept their eggs. The former hypothesis assumes no physical constraints while the latter requires them. We show (1) that most acceptors of Brown-headed Cowbird eggs have small bills, (2) that the single species known to puncture cowbird eggs for ejection also has a small bill, and (3) that all grasp ejectors of Brown-headed Cowbird eggs have large bills. We propose that most acceptors cannot remove cowbird eggs by grasp ejection because their bills are too small. Small hosts probably cannot puncture cowbird eggs for ejection because their unusually thick shells make the costs of puncturing them higher than the benefits of ejection. This hypothesis is capable of explaining the success of cowbirds with scores of host species in the puzzling absence of egg mimicry.     

The nest defence by the red‐backed shrike Lanius collurio – support for the vulnerability hypothesis

The majority of altricial bird species defend their brood against predators more intensively in nestlings rather than eggs stage. Several hypotheses have been proposed to explain this difference. The majority of existing experimental studies have recorded a gradually increasing intensity of nest defence supporting the reproductive value hypothesis. We have compared nest defence in two nesting stages of the red‐backed shrike against two predators of adult birds and against two predators of nests. While the nests with nestlings were defended by parents against three out of four predators, nests with eggs were almost not defended at all. This rapid change in parent nest defence supports rather the vulnerability hypothesis, predicting that the threat to nests with nestlings increases rapidly after hatching, as they became more conspicuous due to their begging and parental provisioning. Unlike most of the species tested previously, the red‐backed shrike uses very vigorous mobbing towards predators. We suggest that the occurrence of this active mobbing (strikes, including physical contact) is a good proxy of the current threat to the nest.     

Development of cardiac rhythms in altricial avian embryos

Mean heart rate (MHR) was determined during incubation and in hatchlings of 14 altricial avian species to investigate (1) if there is a common developmental pattern of heart rate in altricial embryos and (2) if heart rate changes during incubation are correlated with changes in embryonic growth rate. On the basis of normalized incubation MHR increased approximately linearly in 12 of 14 species from as early as 30-40% of incubation to that of pipped embryos. The MHR of hatchlings was equal to or higher than that of pipped embryos in seven species. Passerine embryos and hatchlings maintained higher MHR in comparison to parrots of similar egg mass, which may reflect phylogenetic differences in development. Embryonic MHR increased at a higher rate while embryonic growth rates were highest during the first 40% of incubation in tit, budgerigar and crow embryos than during subsequent development when relative growth rates decreased. MHR became independent of yolk-free wet mass at a smaller fraction of hatchling mass in budgerigar and crow than in the tit, suggesting that MHR is more likely to increase continuously after 40% of incubation in small altricial species than larger species.     

Incubation temperature impacts nestling growth and survival in an open‐cup nesting passerine

For oviparous species such as birds, conditions experienced while in the egg can have long‐lasting effects on the individual. The impact of subtle changes in incubation temperature on nestling development, however, remains poorly understood, especially for open‐cup nesting species with altricial young. To investigate how incubation temperature affects nestling development and survival in such species, we artificially incubated American robin (Turdus migratorius) eggs at 36.1°C (“Low” treatment) and 37.8°C (“High” treatment). Chicks were fostered to same‐age nests upon hatching, and we measured mass, tarsus, and wing length of experimental nestlings and one randomly selected, naturally incubated (“Natural”), foster nest‐mate on days 7 and 10 posthatch. We found significant effects of incubation temperature on incubation duration, growth, and survival, in which experimentally incubated nestlings had shorter incubation periods (10.22, 11.50, and 11.95 days for High, Low, and Natural eggs, respectively), and nestlings from the Low treatment were smaller and had reduced survival compared to High and Natural nestlings. These results highlight the importance of incubation conditions during embryonic development for incubation duration, somatic development, and survival. Moreover, these findings indicate that differences in incubation temperature within the natural range of variation can have important carryover effects on growth and survival in species with altricial young.     

Magellanic Penguin eggshell pores: does number matter?

Most penguin species lay two eggs 3–4 days apart that hatch 1–2 days apart. Hypotheses to explain the shorter incubation period for the second egg include differences in porosity of the eggshells. Eggs with more or larger pores and/or thinner shells have higher gas exchange rates and faster embryonic development. We used eggshells from hatchling Magellanic Penguins Spheniscus magellanicus to test whether eggshell thickness and pore density affect incubation period. We expected: (i) second eggs to have thinner shells and/or more pores than first eggs; (ii) eggs to have thinner shells and/or more pores if they were laid by older females, later in the season, or in burrow nests (more humid than open nests under bushes). We found no support for these hypotheses. Egg pores and shell thickness were not related to incubation period. Eggs from the same clutch were similar in eggshell thickness and pore density. Female age, laying date and nest type were poor predictors of eggshell thickness and pore density. Egg pores, we conclude, have little explanatory power for differences in incubation time of eggs in Magellanic Penguins, and suggest that synchronous onset of incubation matters.     

The effects of shell size and coil orientation on reproduction in female hermit crabs, Clibanarius vittatus

We investigated the effects of shell coil orientation and shell size on reproduction in field populations of the hermit crab, Clibanarius vittatus. Females were collected in the intertidal in Beaufort, NC. Shell parameters were measured and size (cephalothorax length) and reproductive status were determined for 70 females occupying Busycon shells. Crabs were categorized as berried (eggs on the pleopods), mature ovaries, or non-reproductive (no eggs). For berried females, the number of eggs was recorded. By offering a separate group of females access to empty shells, it was possible to calculate optimal shell size and the deficit in shell size for field-collected animals.Females that were berried were in shells closer to the optimal shell size than females with mature ovaries, both for shell weight and shell volume. And females with mature ovaries were in shells that were closer to the optimal size than females that were non-reproductive. For both categories of females without eggs on the pleopods, the majority of females were in shells that were too big (in weight and internal volume). While the percentage of berried females did not differ between dextral (Busycon carica) and sinistral (Busycon sinistrum) shells, the non-reproductive females had a much smaller deficit in volume in sinistral shells compared to dextral shells. For berried females, there was no relationship between the magnitude of their shell deficit and the number of eggs carried. Our results suggest that reproduction is inhibited when females occupy shells sufficiently greater than the optimal shell size.     

Influence of temperature on hatching of eggs of Lepidurus couesii (Crustacea,Notostraca)

Tadpole shrimps (Notostraca) occur sporadically in temporary ponds and their survival there depends largely upon the drought-resistant eggs they produce. Environmental conditions conducive to hatching of eggs of Lepidurus couesii were investigated in the laboratory. Almost all eggs hatched best at 20 °C, whether desiccated for a short or long period, with a prior freezing shock or without such a shock, with intact shells. Eggs that endured a longer period of desiccation and eggs with abraded shells displayed a more equivocal response to different temperatures for hatching. Long-term hatchability of eggs was demonstrated. Time required for successful hatching was shortest at 20 °C, with no discernible difference between 17 °C and 25 °C. Both short- and long-term survival of populations of the species appears to be fostered by the adaptive response to temperature shown by the eggs.     

Changes in egg shell characteristics of the Sparrowhawk (Accipiter nisus) and Peregrine (Falco peregrinus) associated with exposure to environmental pollutants during recent decades

In Britain since the late 1940s, the Sparrowhawk ( Accipiter nisus ) and Peregrine (Falco peregrinus) have laid eggs with unusually thin shells. DDT and its metabolites have been blamed. This paper reports how various properties of modern shells differ from those of older shells of normal thickness.
For the shells of both species, there were roughly proportional reductions in thickness of the two main component layers, the mammillary and palisade layers, suggesting that thin shells resulted from a decreased rate of deposition. In addition, in modern Sparrowhawk shells, the resistant surface layer was especially deficient perhaps due to a further reduction in deposition rate or to slight premature termination. Shell thinning was associated with a proportionately greater decrease in shell strength. For the Peregrine, porosity, measured as the rate of passage of water vapour, was lower for the thin shells than for normal shells. This difference could not be explained by a change in the area of the pore channels, since the modern shells did not have fewer pores and the pore channels were the same size and shape in the two samples of shells. However, in the thin shells of both species, mammillae height increased relative to mammillary layer thickness, and in the Peregrine shells the extent of this increase was related to the change in porosity.     

Variation in the developmental timing of flight-feather growth in nestling birds

The timing of primary-feather development in relation to growth in body-mass varies considerably between altricial species. This variation relates, at least in part, to differences in nesting habits: species nesting in relatively well-protected nest sites, such as holes, start primary-feather development later than altricial species using open-cup nests. For the latter 'open-nesting' species, the timing of primary-feather development also tends to show an allometric correlation with adult body-size. Since primary-feather development takes longer, rerative to growth in body-mass, in small species than in large ones, these data suggest that, for small species, there will be an important selective advantage in using relatively secure nest sites.