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.     

A comparative study of changes in the fine structure of avian eggshells during incubation

A scanning electron microscope study of the morphological changes which occur in shells of hen and quail eggs during incubation is described. The results are compared with observations on the shells of hatched eggs taken from a range of species. It was found that less change occurred in the shells of altricial species than precocial ones, the difference being associated presumably with a smaller calcium requirement for developing altricial embryos. The cores rather than the sides of mammillae appeared to be the major sites of erosion.     

Structure of shells from eggs of kinosternid turtles

Shells from eggs of five species of kinosternid turtle (Sternotherus minor, Kinosternon flavescens, K. baurii, K. Hirtipes, and K. alamosae) were examined with light and scanning electron microscopy. Except for possible differences among species in thickness of eggshells, structure of shells from all eggs was similiar. In general, kinosternid turtles lay eggs having a rigid calcareous layer composed of calcium carbonate in the form of aragonite. The calcareous layer is organized into individual shell units with needlelike crystallites radiating from a common center. Most of the thickness of the eggshell is attributable to the calcareous layer, with the fibrous shell membrane comprising only a small fraction of shell thickness. Pores are found in the calcareous layer, but they are not numereous. The outer surface of the eggshells is sculptured and may have a thick, organic layer in places. The outer surface of the shell membrane of decalcified eggshells is studded with spherical cores which presumably nucleate growth of shell units during shell formation. The shell membrane detaches from eggs incubated to hatching, carrying with it remnants of the calcareous layer. Such changes in shell structure presumably reflect withdrawal of calcium from the eggshell by developing embryos.     

Cardiomyocyte ploidy levels in birds with different growth rates

Cytofluorimetric study of ploidy levels in ventricular cardiomyocytes was carried out on 36 adult bird species belonging to 10 orders as well as on the quail Coturnix coturnix, of different ages. It was shown that polyploidization of quail cardiomyocytes occurs during the first 40 days after hatching and ends by the time growth is completed. In adult birds, the cardiomyocyte ploidy hardly changed at all. Interspecies comparison revealed that in the adult bird myocardium 2cx2 myocytes are predominant, accounting for at least 50% of the cell population. Multinuclear cells with three to eight diploid nuclei were widespread. The percentage of such cells was five to six times higher in precocial species than in altricial birds of the same weight. Myocytes with polyploid nuclei were rare. A significant interspecies variability of cardiomyocyte ploidy levels was observed. The most prominent differences were found between the precocial and the altricial birds. The mean number of genomes in cells correlated both with the body mass and with the growth rate of the birds. The differences between the precocial and altricial birds disappeared when a statistical method was used to eliminate the effect of the growth rate, but did not when the effect of body mass was eliminated. Among the altricial birds, which are generally immobile during growth, the cardiomyocyte ploidy levels also correlated more closely with growth rate than with body mass. The opposite was observed in the precocial birds, which are highly mobile from the first minutes of life. We conclude that the interspecies variability of bird cardiomyocyte ploidy levels is a result of changes in the balance between the cardiac functional load and the growth rate; this is manifested at the cellular level as a competition between the proliferation and differentiation of cardiomyocytes. J. Exp. Zool. 289:48-58, 2001.     

Embryonic Calls as Care-soliciting Signals in Budgerigars,Melopsittacus undulatus

Embryonic calls occur 1–3 d before hatching among precocial and some altricial birds. In precocial species, calls may synchronize hatching among siblings or, in semi-precocial species, elicit parental attention to, and often thermoregulation of, the hatching egg. Much less is known about the functional significance of calls in fully altricial species. In this study, naturalistic observations and laboratory experiments were used to document factors affecting calling and the parental responses to calls in one altricial species, the budgerigar Melopsittacus undulatus. Budgerigar chicks hatch asynchronously and vocalize 24–48 h before hatching. Embryonic calling rates increase at higher egg temperatures, and also as embryos near hatching. Parents easily locate a calling egg in their clutch, even among a large brood of much older, vocalizing nestlings. Furthermore, they actively assist in the last stages of hatching by helping to break the shell along the crack in the egg. Both observational and experimental evidence suggests that embryonic vocalizations are distinctive signals that increase parental attention and care, and may stimulate hatching assistance to a calling 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.     

A comparative study of embryonic development of some bird species with different patterns of postnatal growth

Some studies show that birds with high postnatal growth rates (e.g. altricial species) are characterized by a rapid early development of "supply" organs, such as digestive organs. Birds with low postnatal growth rates (e.g. precocial species) exhibit a slower early development of these organs and a more rapid early development of other "demand" organs, such as brain, muscles, skeleton and feathers. To test whether these differences can be traced back to early embryonic development and whether they can be associated with changes in developmental timing, i.e. heterochrony, we compared embryos of the precocial quail and the altricial fieldfare, two bird species with low and high postnatal growth rates, respectively. We used classical staging techniques that use developmental landmarks to categorize embryonic maturity as well as morphological measurements. These techniques were combined with immune detection of muscle specific proteins in the somites. Our data showed that the anlagen of the head, brain and eyes develop earlier in the quail than in the fieldfare in contrast to the gut which develops earlier in the fieldfare than in the quail. Our data also showed that the quail and the fieldfare displayed different rates of myotome formation in the somites which contribute to muscle formation in the limbs and thorax. We believe these observations are connected with important differences in neonatal characteristics, such as the size of the brain, eyes, organs for locomotion and digestion. This leads us to the conclusion that selection for late ontogenetic characteristics can alter early embryonic development and that growth rate is of fundamental importance for the patterning of avian embryonic development. It also appears that this comparative system offers excellent opportunities to test hypotheses about heterochrony.     

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.     

Comparative growth rates and oxygen consumption in young Galliformes

The high correlation between growth rate and adult body weight has been much more thoroughly documented for altricial birds than for precocial species. This paper gathers data from the literature for precocial Galliformes and also reports new growth data on six galliform species for analysis. The onset of homeothermic ability is investigated in Galliformes over a range of body size. The results confirm that (1) large species' chicks grow at a slower rate than those of smaller species, and (2) larger species' chicks can thermoregulate earlier than smaller species' chicks under cold stress situations. Published embryonic body weights are also analysed to determine when growth rate differences appear in the development of precocial species. No interspecific differences appeared in the relative growth rates of embryos, and therefore species body size does not appear to influence growth rate before hatching.     

Timing of incorporation of docosahexaenoic acid into brain and muscle phospholipids during precocial and altricial modes of avian development

We investigated the possibilities that the proportion of docosahexaenoic acid (DHA) in phospholipids of brain and skeletal muscle at hatch, and the ontogenetic timing of the DHA accretion spurt in these tissues, might serve as indices of neonatal functional maturity that discriminate between precocial and altricial avian developmental modes. Comparison of the fatty acid profiles of the initial and residual yolks of two free-living altricial species, the swallow (Hirundo rustica) and the sparrow (Passer domesticus), reveals that, in contrast to precocial birds, there is no preferential uptake of DHA from the yolk during embryonic development. At hatch, the proportions of DHA in brain phospholipid (wt.% of fatty acids) of the swallow and sparrow, at 8.1% and 5.0%, respectively, are far lower than the values (16.9-19.6%) reported for non-altricial species. This reflects a marked difference in the timing of the brain DHA accretion spurt, which occurs during the first half of the embryonic period of precocial birds, but is largely delayed until after hatching in the altricial species. By the time of fledging, the proportion of DHA in the swallow brain phospholipid has increased to 14.3%. For non-altricial birds, the brain DHA concentration at hatch shows little interspecies variation, despite major differences in yolk DHA content. The proportions of DHA in leg muscle phospholipid of the newly hatched swallow and sparrow, at 2.9% and 2.5%, respectively, are far lower than the value (6.7%) for the precocial chicken. Again, this relates to differences in developmental timing, with muscle DHA accretion occurring in the first half of the chicken's embryonic period, whereas, in the swallow, this increase is delayed until after hatching. By the time of fledging in the swallow, DHA forms 9.3% of muscle phospholipid fatty acids, equivalent to the level attained in chicken muscle at the mid-embryo stage. The results indicate a clear distinction between altricial and non-altricial avian species in the timing of tissue DHA accretion during development, presumably reflecting differences in neonatal functional maturity.     

Intraclutch Hatch Synchronization in Pheasants and Mallard Ducks

Synchronization of hatching within clutches of precocial bird species can be achieved either by acceleration or retardation, i.e. by shortening or prolonging the incubation period. The ability of mallard ( Anas platyrhynchos ) and ring-necked pheasant ( Phasianus colchicus ) embryos to accelerate or retard hatching was tested by incubating separate clutches, of which three eggs had 2 d longer or shorter incubation time than the others, and observing their individual time of pipping (breaking of the shell). Mallard embryos were able to delay hatching by on average 0.6 d (43% of the eggs delayed at least 1 d), but were better at acceleration (on average 1.3 d; 91% of the eggs accelerated more than 1 d). Conversely, pheasant embryos were only able to accelerate by 0.4 d (50% accelerated more than 1 d), but were better at delaying the hatching (1.2 days; 77% delayed more than 1 d). This difference between the species may depend on different degrees of relatedness within clutches in pheasants and mallards. It may also be an effect of the more developed sensory and neuromuscular systems in galliforms; a reduction of the incubation period would mean that the development of, for example, locomotion would be insufficient at hatching.     

When to be born? Prolonged pregnancy or incubation enhances locomotor performance in neonatal lizards (Scincidae)

The degree of offspring development at hatching (or birth) varies among species within most major vertebrate lineages; altricial vs. precocial birds offer the clearest example of a trade-off between early hatching and the degree of locomotor development of the hatchling. No such diversity has been reported for reptiles, but we suggest that natural selection may fine-tune the time of hatching (in oviparous species) or birth (in viviparous species) to optimize offspring phenotypes and hence, maximize fitness. This hypothesis predicts enhanced neonatal performance after more prolonged incubation or gestation, within as well as among populations. Both published and original data on Australian scincid lizards support this prediction. In a field study, viviparous alpine skinks (Niveoscincus microlepidotus) that gave birth later in the season had faster-running offspring, that had a higher probability of surviving through the first year of life. The enhanced performance and survival were not secondary results of larger offspring size. After controlling for effects of mean incubation temperature, prolonged development also correlated with enhanced locomotor performance in hatchlings from eggs of an oviparous skink (Bassiana duperreyi) incubated at warm temperatures (> 20 degrees C) but not at cooler temperatures (< 20 degrees C). We suggest that embryonic reptiles control their date of hatching or birth and thus, their stage of development at this critical life-history transition.     

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]     

Of fleas and geese: the impact of an increasing nest ectoparasite on reproductive success

Past studies on the relationship between nest ectoparasites and avian fitness have been primarily limited to altricial hosts. Life history strategies of precocial and altricial birds vary considerably, limiting our ability to infer the effect of nest parasites on fitness of precocial species. Ross's Chen rossii and lesser snow goose Chen caerulescens caerulescens populations have been growing at unprecedented high rates. New limiting factors on vital rates of these precocial birds may arise after populations have been released from previously regulating factors. The flea Ceratophyllus vagabundus vagabundus is an apparently newly emerging nest parasite in the arctic goose colony at Karrak Lake, Nunavut, Canada. We examined the relationship between flea abundance (measured by the proportion of goose eggs covered by blood in each nest) and goose reproductive success from 2001–2004. In three of four years of study, nest success was inversely related to flea abundance in nests. Despite the potential for high costs to individuals, the overall effects of fleas on goose nesting success have thus far been small. We demonstrated that nest parasites negatively influence reproductive success of precocial bird hosts despite host life history strategy of leaving the nest quickly after hatch, which results in minimal exposure to nest parasites compared to altricial birds that raise their young in the nest.     

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.     

Developmental basis for telencephalon expansion in waterfowl: enlargement prior to neurogenesis

Some altricial and some precocial species of birds have evolved enlarged telencephalons compared with other birds. Previous work has shown that finches and parakeets, two species that hatch in an immature (i.e. altricial) state, enlarged their telencephalon by delaying telencephalic neurogenesis. To determine whether species that hatch in a relatively mature (i.e. precocial) state also enlarged their telencephalon by delaying telencephalic neurogenesis, we examined brain development in geese, ducks, turkeys and chickens, which are all precocial. Whereas the telencephalon occupies less than 55 per cent of the brain in chickens and turkeys, it occupies more than 65 per cent in ducks and geese. To determine how these species differences in adult brain region proportions arise during development, we examined brain maturation (i.e. neurogenesis timing) and estimated telencephalon, tectum and medulla volumes from serial Nissl-stained sections in the four species. We found that incubation time predicts the timing of neurogenesis in all major brain regions and that the telencephalon is proportionally larger in ducks and geese before telencephalic neurogenesis begins. These findings demonstrate that the expansion of the telencephalon in ducks and geese is achieved by altering development prior to neurogenesis onset. Thus, precocial and altricial species evolved different developmental strategies to expand their telencephalon.     

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.     

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.     

On the optimal growth of the alimentary tract in avian postembryonic development

It was shown in the mathematical model described elsewhere that when growth rate of the chicks is maximized and not constrained by the food availability, the optimal relationship between body mass and alimentary tract mass should conform to a single straight line, or two-, or three-segmented straight lines. Here, we present the data on growth of 11 bird species, and we test the model using the mass of intestines as an indicator of growth of the alimentary tract. The results support the predictions of the model for altricial species and contradict them for precocials. Since precocial species examined here were not food-limited, we suggest that the lack of optimal growth of their alimentary tract is inherent to their mode of development. This may account for their lower growth rate, as compared to altricials. The existence of the optimal growth of the alimentary tract in altricial nestlings suggests that under natural conditions the food is much more abundant than it is generally assumed.     

A comparative study of the ultrastructure and mineralogy of calcified land snail eggs (Pulmonata: Stylommatophora)

This study indicates that eggs containing calcium carbonate crystals occur in at least 36 of the 65 known families of the land snails (class Gastropoda: order Stylommatophora). Eggs from 22 of these families were available for examination. The x-ray diffraction data, available for the first time for 21 of these families, shows that these egg shells are all made of calcite only, or of a combination of calcite with smaller amounts of aragonite. All of the snail (body) shells examined were made of aragonite only. This is the first ultrastructural investigation of these egg shells, and it indicates that the eggs exhibit enough structural diversity to allow identification of parental animals to genus, and often to species level solely on the basis of egg shell ultrastructure. All of the calcified eggs may be divided into two groups: (1) partly calcified, with discrete crystals of CaCo₃ dispersed in the jelly layer, and (2) heavily calcified, with a hard, brittle egg shell made of fused crystals of CaCO₃ much like an avian egg. Both types of calcified eggs occur in oviparous as well as in ovoviviparous snails. Because of the wide distribution of calcified eggs in the Stylommatophora, and because of the occurrence of heavily calcified eggs in ancient families such as Partulidae, Endodontidae, and Zonitidae, the calcified egg is viewed as a primitive land snail trait associated with terrestrial adaptation. The function of the calcified egg shell, in addition to mechanical support of egg contents, is to supply the developing embryo with enough calcium to form the embryonic shell by the time of hatching.