The source of the nutrients required for egg production in zebra finches Poephila guttata

The source of nutrients used for egg formation are poorly known for most bird species. This study of the zebra finch Poephila guttata showed that food intake did not increase during egg production, but the decline in female body reserves of protein and fat were sufficient to account for most of the nutrients in a clutch of four eggs. Female birds significantly reduced their activity levels during ova enlargement, which may play a role in diverting resources to egg production. Birds increased their intake of calcium-rich food items when eggs were being laid, and this intake accounted for all the calcium needed for eggshell formation. The zebra finch depends heavily on stored body reserves for egg formation, which is probably unusual in small passerines.     

Individual quality and food availability determine yolk and egg mass and egg composition in tree swallows Tachycineta bicolor

Variation in egg size and composition can have important consequences for the quality of offspring. We investigated the factors influencing the yolk mass and egg mass of tree swallows breeding in Ithaca, NY. Using a nondestructive technique to estimate yolk mass via standardized digital-candler photographs, we compared yolk size and egg size of tree swallows Tachycineta bicolor in response to variation in food availability and individual quality. Insect availability one to three days prior to laying, but not four to six days, predicted yolk mass, while insect availability two to three days prior to laying predicted total egg mass. This suggests that, while eggs are formed over longer periods, food availability closer to time of laying has the greatest influence on egg size. These results were supported by collected eggs, as yolk rings revealed that tree swallow eggs are formed over 5–6 days. There was an influence of female quality as well, with early laying birds, independent of food availability, laying larger eggs. Eggs laid later in the laying sequence had larger yolks and greater egg mass. Overall, variation in egg quality appears to be due to a combination of environmental conditions, reflected in food resources, individual quality, and allocation tradeoffs during the laying period.     

Tissue mass dynamics during egg-production in female Zebra Finches Taeniopygia guttata: dietary and hormonal manipulations

Changes in tissue masses associated with egg production were investigated in female Zebra Finches Taeniopygia gutatta using dietary and hormonal manipulations. We tested three hypotheses: that changes in organ masses, (a) reflect utilisation of endogenous nutrient stores due to inadequate daily dietary intake, (b) involve changes in organ structure or 'functional capacity', and (c) are initiated by onset of reproductive development (e.g. elevated plasma estrogen or yolk precursor levels, oviduct growth). Pectoral muscle lean dry mass was 18–22% lower in breeding females at the 1-egg stage compared to non-breeders, and this was independent of nutritional plane, i.e. similar changes occurred in birds provided with supplemental protein or egg food. Heart lean dry mass was also lower (16%) in breeding females, but only in birds on a low-quality seed diet, not in birds on supplemented diets. Decreases in total liver mass (14%) were due to changes in lipid content not lean dry mass, and were diet-dependent. These results demonstrate that changes in organ masses associated with egg production are complex, and do not simply reflect a general mobilisation of stored protein. We discuss why there is no hypertrophy of biosynthetic or metabolic 'machinery' associated with egg production in birds (cf. reproducing mammals). Exogenous 17β-estradiol induced plasma levels of yolk precursors typical of breeding birds, and initiated oviduct growth (to 31% of mature size). However, estradiol treatment caused no change in mass of pectoral muscle, heart or liver, demonstrating that there is no simple relationship between onset of reproductive development and associated tissue mass changes.     

Eggs, egg formation and the timing of breeding

The eggs of birds contain all the nutrients necessary for the developing embryo. The female has to obtain these nutrients, and while in some species these may be gathered and stored over a period of time, in many species they seem to be obtained on a daily basis. Obtaining the calcium necessary for the eggshell may pose special problems for some species, which may have to give up valuable feeding time in order to search for calcium.
Egg size varies considerably, even within species, and the reasons for this are not clear. In the Great Tit Parus major , large eggs produce nestlings which have a higher chance of hatching, surviving to fledging and surviving after fledging. However, large eggs require the female to acquire more nutrients to form them, and large chicks may sometimes be at a disadvantage. The amount of energy required to form a larger egg often seems small unless the metabolic costs of egg formation are taken into account.     

Eggs, egg formation and the timing of breeding

The eggs of birds contain all the nutrients necessary for the developing embryo. The female has to obtain these nutrients, and while in some species these may be gathered and stored over a period of time, in many species they seem to be obtained on a daily basis. Obtaining the calcium necessary for the eggshell may pose special problems for some species, which may have to give up valuable feeding time in order to search for calcium.
Egg size varies considerably, even within species, and the reasons for this are not clear. In the Great Tit Pants major, large eggs produce nestlings which have a higher chance of hatching, surviving to fledging and surviving after fledging. However, large eggs require the female to acquire more nutrients to form them, and large chicks may sometimes be at a disadvantage. The amount of energy required to form a larger egg often seems small unless the metabolic costs of egg formation are taken into account.     

Seasonal changes in egg-mass within and among clutches of birds: general explanations and a field study of the Blackbird Turdus merula

In many populations of birds there is a seasonal change in the mean mass of eggs in the clutch. This might be caused by seasonal changes in the costs of egg-production, or changes in the benefits of laying eggs of different size. In the Blackbird Turdus merula the mean mass of an egg correlated specifically with the air temperature during the period when it was predicted to be undergoing rapid follicular growth. There was no residual effect of date or day-length on egg-mass when statistically controlling for temperature during the period of rapid yolk synthesis, yet temperature still had a significant effect when controlling for date or day- length. Thus the seasonal increase in egg-mass appears to be due to changes in the cost of egg-production, not changes in the benefits of laying larger eggs. However, I could find no effect of food supply during laying on the mean mass of eggs in the clutch, either using an indirect measure of food availability, rainfall, or in a food-supplementation experiment. This could be because females responded to extra food by laying earlier, and probably larger, clutches, rather than by increasing egg-mass. The effect of temperature on egg-mass increased through the laying sequence and there was a small seasonal increase in the mass of the last-laid egg compared with the mean of the other eggs in the clutch. I propose that the mean mass of the last-laid egg relative to the clutch mean, which can characterize a species or population, could evolve in response to the environmentally-caused variance in the mass of the last-laid egg: when the variance is high, the mean may have to be high to avoid producing unviable eggs.     

Maternal adjustment or constraint: differential effects of food availability on maternal deposition of macro‐nutrients,steroids and thyroid hormones in rock pigeon eggs

In oviparous species like birds, eggs provide the direct environment in which embryos are developing. Mothers may adjust different egg components in different ways in reaction to environmental cues either to adjust offspring development or because of constraints. In this study, we investigated the effects of food quality and quantity before and during egg laying on three different aspects of egg quality: macro‐nutrients (egg and yolk mass), androgens (testosterone and androstenedione), and thyroid hormones (3,5,3′‐triiodothyronine, T3 and l ‐thyroxine, T4), using the rock pigeon (Columba livia). As expected, egg and yolk mass were significantly reduced for the eggs laid under the poor‐food condition, indicating a maternal trade‐off between offspring and self in allocating important resources. We did not find any significant change in yolk testosterone or their within‐clutch pattern over the laying sequence. This is consistent with the fact that, in contrast with nutrients, these hormones are not costly to produce, but does not support the hypothesis that they play a role in adjusting brood size to food conditions. In contrast, we found that T3 levels were higher in the egg yolks under the poor‐food condition whereas the total T4 content was lower. This change could be related to the fact that iodine, the critical constituent of thyroid hormones, might be a limiting factor in the production of this hormone. Given the knowledge that food restriction usually lead to reduction of circulating T3 levels, our results suggested that avian mothers can independently regulate its concentrations in their eggs from their own circulation. The study demonstrates that environmentally induced maternal effects via the egg can be a result of a combination of constrained resources and unconstrained signals and that thyroid hormones might be an interesting case of both. Therefore, this hormone and the interplay of different maternal effects on the offspring phenotype deserve much more attention.     

Effects of temperature and season on egg size, hatchling size and adult size in Notiophilus biguttatus

1. Temperature-induced egg size variation and its effects on successive life stages in the carabid beetle Notiophilus biguttatus were examined.
2. In the laboratory, across temperature regimes, egg size and number were inversely related; number of eggs and total egg mass were higher, but egg size was smaller at high temperatures.
3. Food intake rate was shown not to be involved in the temperature effect on egg size.
4. Within the higher temperature regimes, among females, egg size was negatively correlated with number of eggs and with total egg mass.
5. Data on egg mortality and egg development time did not explain why at low temperature eggs were larger than at high temperature.
6. Larvae hatching from eggs produced at a low temperature were heavier than larvae from eggs produced at a high temperature, irrespective of temperature during development.
7. In a prolonged outdoor experiment (January – July), encompassing the main breeding period of N. biguttatus , egg size decreased and both egg production rate and total egg mass increased in the course of the experiment.
8. In the field, an effect of seasonal change in temperature on adult body size was found; teneral beetles that had their juvenile period early in the season were larger than those that had their juvenile period later in the season.
9. The results of the study suggest a mechanistic explanation in which the egg size response to temperature follows from a difference in temperature sensitivity between two processes in oogenesis; adaptiveness of the temperature response was not clarified.     

The effect of maternal state on the steroid and macronutrient content of lesser black-backed gull eggs

It has been proposed that female birds can influence the phenotype of their offspring by provisioning eggs with variable amounts of nutrients and maternal hormones. Egg quality is strongly influenced by maternal body reserves and the amount of food available at the time of egg formation. This study investigated the effects of maternal state and food availability on the capacity of female lesser black-backed gulls Larus fuscus to provision their eggs with macronutrients and steroid hormones. Maternal state was reduced by increasing egg-production effort, whereas extra food was provided to reverse this effect. Compared with eggs of first clutches, eggs of experimentally induced replacement clutches exhibited a lower yolk/albumen ratio and contained more yolk testosterone. During one of the three years in which the study was performed, replacement eggs also contained more 17β-estradiol. Food provisioning during the relaying interval did not affect changes in yolk/albumen ratio or steroid concentrations, but fed females produced bigger eggs in their replacement clutch. This study demonstrates significant within-female consistency in egg size, macronutrient content, and yolk steroid concentration, and it shows that these egg characteristics are influenced by maternal state, food availability, and the timing of breeding.     

Fecundity, lifespan and egg mass in butterflies: effects of male-derived nutrients and female size

1. Effects of larval reserves and nutrients received as adults on fecundity and lifespan in female Danaus plexippus (the Monarch Butterfly) were measured to determine the relative importance of different sources of nutrients for reproduction and somatic maintenance.
2. Egg-laying lifespan was correlated with female size but not with the amount of male-derived nutrients or adult food concentration.
3. Lifetime fecundity was higher when females received a large first spermatophore, but was not affected by female size when lifespan was controlled or by adult food concentration.
4. At the end of their lives, females contained unlaid eggs and retained, on average, 88% of their initial mass. This proportion was unchanged in two years, although mean egg-laying lifespan varied from 22·5 to 28·7 days.
5. Egg mass decreased over the female lifespan, and was correlated with female size.
6. These results suggest that larval reserves are more important for somatic maintenance than adult income, but that the protein-rich nutrients received from males contribute to egg production. This supports theoretical predictions and empirical studies of other Lepidoptera showing that larval reserves are less likely to affect fecundity when the adult income can contribute substantially to egg production.     

Intermittent fasting during winter and spring affects body composition and reproduction of a migratory duck

We compared food intake, body mass and body composition of male and female black ducks (Anas rubripes) during winter (January-March). Birds were fed the same complete diet ad libitum on consecutive days each week without fasting (control; nine male; nine female) or with either short fasts (2 day x week(-1); nine male; nine female), or long fasts (4 day x week(-1); eleven male; twelve female). We continued treatments through spring (March-May) to measure the effect of intermittent fasts on body mass and egg production. Daily food intake of fasted birds was up to four times that of unfasted birds. Weekly food intake of males was similar among treatments (364 g x kg(-1) x week(-1)) but fasted females consumed more than unfasted females in January (363 g x kg(-1) x week(-1) vs. 225 g x kg(-1) x week(-1)). Although both sexes lost 10-14% body mass, fasted females lost less mass and lipid than unfasted females during winter. Total body nitrogen was conserved over winter in both sexes even though the heart and spleen lost mass while the reproductive tract and liver gained mass. Intermittent fasting increased liver, intestinal tissue and digesta mass of females but not of males. Fasting delayed egg production in spring but did not affect size, fertility or hatching of the clutch. Females on long fasts were still heavier than controls after laying eggs. Thus black ducks combine flexibility of food intake with plasticity of digestive tract, liver and adipose tissue when food supply is interrupted during winter. Females modulate body mass for survival and defer reproduction when food supply is interrupted in spring.     

Fatty acid signatures of female Brünnich's guillemots Uria lomvia suggests reliance on local prey for replacement egg production

The laying of smaller replacement eggs has been described as a time-saving adaptation because chicks generally grow faster once hatched than inside the egg. However, chicks hatched from smaller eggs have, potentially, lower survival. Consequently, the smaller replacement egg represents a benefit to the female in terms of preserving its own condition at a cost to their offspring. We test these ideas by measuring adult mass changes and plasma lipid concentration changes in male and female Brünnich's guillemots Uria lomvia breeding on Coats Island, Nunavut. Though males lost more mass than females, these differences were not significant. Between laying the first and replacement egg, plasma fatty acid concentrations declined in females and increased in males, suggesting that females mobilise less lipid to preserve their condition after laying the replacement egg. In females, plasma lipid concentrations of the dominant fatty acids found in the eggs (16:0 and 18:1) declined between the laying of first and replacement eggs while plasma concentrations of 20:1 increased in both males and females. We compared the fatty acid signatures of first and replacement egg to look for evidence of differences between the lipid sources for their production. Principal component and discriminant function analyses showed that the fatty acid signatures of replacement eggs were closer to the signatures of the local prey than those of first eggs. We suggest that females rely on local sources of energy to a greater degree for the production of the replacement egg than the first egg, but that endogenous reserves of certain nutrients are important for the production of both eggs.     

Relative contribution of lipid sources to eggs of lesser scaup

Studies of how birds mobilize nutrients to eggs have traditionally considered a continuum of possible allocation strategies ranging from income breeding (rely on food sources found on the breeding grounds) to capital breeding (rely on body reserves stored prior to the breeding season). For capital breeding, stored body reserves can be acquired either on or away from the breeding grounds, but it has been difficult to quantify the relative contribution of each, precluding identification of key habitats for acquiring nutrients for clutch formation. During 2006–2009, we explored the importance of spring‐staging habitats versus breeding‐area habitats for egg‐lipid formation in female lesser scaup Aythya affinis using stable carbon (δ¹³C) isotope analyses. Although δ¹³C values for abdominal lipid reserves brought to the breeding grounds overlapped those of local amphipods, we were able to quantify the importance of local plant carbohydrates (seeds of emergent wetland plants) to the production of eggs. We compared the importance of local wetland seeds (overall δ¹³C: ?29.1 ± 0.9‰ SD) to combined lipid stores and lipids from local amphipods (overall δ¹³C: ?23.8 ± 2.2‰). Local seeds and stored body lipids contributed equally to egg lipid formation across years but we found evidence of annual variation in their relative importance. Wetland seeds contributed 39% (SE = 10%) to egg lipid production, and the importance of this source varied by year (90% CI = 47–75% in 2006, 13–42% in 2007, 29–65% in 2008, and 7–30% in 2009). In contrast to earlier studies that suggest lesser scaup predominantly employ a capital breeding strategy, our results suggest that in some years females may attain half of their energy for clutch formation from foods on the breeding grounds.     

Production and egg quality in layers fed organic diets with mussel meal

The first limiting nutrients in typical laying hen diets are the sulphur-containing amino acids and, in particular, methionine. To fulfil the birds' recommended requirement, conventional diets are supplemented with synthetic methionine. As this is not allowed in organic production it becomes very important to have access to alternative high-quality protein feed ingredients. An experiment was performed to evaluate the possibility to compose a diet with 100% organically approved feed ingredients using mussel meal as a major source of methionine. The experiment included 678 Lohman Selected Leghorn (LSL) and 678 Hyline White, W-98, layers during 20 to 72 weeks of age. There were 12 aviary pens with 113 birds in each. The birds were fed one of the two experimental diets containing either 3.5% or 7% dried mussel meat meal or a commercial organic diet from a Swedish feed manufacturer for comparison. Production and mortality were recorded daily per group, and egg weight was recorded once weekly. At 33, 55 and 70 weeks, 10 eggs from each treatment group were collected and analysed for internal egg quality. Diets had no significant effect on laying percentage, egg mass, feed intake, feed conversion ratio, mortality, bird live weight or proportion misplaced, cracked or dirty eggs. Egg quality, that is, shell deformation, shell breaking strength, albumen height, shell percentage and proportion of blood and meat spots were also unaffected. There was a significant difference in egg yolk pigmentation, that is, the egg yolk was more coloured when feeding 7% mussel meal compared with the other diets. Hyline hens had lower feed intake and laying percentage, and higher egg weight, but lower egg mass production than LSL birds. The age of the birds influenced all egg quality traits except for meat and blood spots. The dry matter of the excreta was significantly lower for both genotypes fed the 7% mussel meal diet. These results indicate that mussels may be a high-quality protein source and may replace fishmeal in organic diets for layers.     

Factors determining persistent asymmetry and egg shape in birds: A hypothesis

The shape of birds' eggs has fascinated scientists for many years. It is now possible mathematically to describe shape accurately, allowing exploration of the physical and ecological factors driving the evolution of egg shape. However, there has been relatively little consideration of how egg shape is established in the oviduct or, given that even without an external calcitic layer eggs retain their shape, how shape is fixed in the isthmus. This paper proposes a hypothesis that attempts to explain how egg shape is established and fixed in the oviduct. The hypothesis suggests that as the egg mass (i.e. yolk and albumen) moves from the magnum into the isthmus, it is squeezed by the physical restriction imposed by the isthmus lumen and cannot easily move into the isthmus. As the leading edge of the egg mass enters the isthmus, the egg mass in the distal magnum is forced to bulge outwards, resulting in an asymmetrical shape. The various egg shapes observed in birds are, hence, produced by the interaction between the size of the egg mass relative to female body mass, and the degree of the restriction of the isthmus. Thus, a large egg mass, i.e. relative to female body mass, entering a narrow isthmus will produce a pointed egg shape. If the egg mass is relatively small, and the isthmus lumen wide, more of the egg mass could enter the isthmus and the degree of asymmetry would be reduced. It is further proposed that egg shape is fixed during the formation of the shell membranes in the isthmus because the constituent protein fibres permanently stick together as they are deposited. For the first time this hypothesis helps explain the pattern of deposition and characteristics of the calcitic egg in relation to the diversity of egg shapes in birds and reptiles.     

Body reserves and nutritional needs during laying preparation in barn owls

To investigate the composition of the body reserves made during pre-laying by breeding European barn owls (Tyto alba), we have analysed the body composition of captive breeding and non-breeding females sacrificed during the laying period. The data obtained were compared to the daily requirement for egg formation obtained by an egg composition analysis and the timing of egg synthesis. This study demonstrates that body mass gain observed in breeding females (+38.3 g after eggs in formation and gonadal tractus were removed) was not the consequence of an accumulation of body fuels like lipids but of mainly water and lean material. The lipidic reserves were found to be less important in breeding than in non-breeding females and their localisation modified; lipids were absent from medullar bones in breeding females which liberated room for other storage. The subcutaneous tissue, which was homogeneous in non-breeding females, was located principally under the brood patch in breeding females. Nutrients and energy required during egg formation could be obtained without modification of daily food intake. These results show that a laying event can be initiated in 14 days and that the onset of reproduction is not triggered by body condition in barn owls. The water accumulation observed is suggested to be the mere consequence of an increase of protein metabolism (egg and moult). These results intimate that the body mass increase observed in diurnal and nocturnal raptors during laying preparation, interpreted as an energy safety strategy, ought to be reconsidered. Accepted: 25 February 2000     

Chick development in free-living great tits Parus major in relation to calcium availability and egg composition

Evidence from a number of avian studies suggests that limitation of exogenous calcium (Ca) may reduce egg quality and retard nestling growth. However, it is poorly understood whether reduction in chick growth in Ca-poor areas is due to insufficient intake of dietary Ca or caused by maternal Ca limitation mediated through subtle changes in composition of eggs. In this study, we provide new evidence that Ca availability during egg formation may indeed affect egg composition and influence chick development of the great tit Parus major at early developmental stages. Ca-supplemented birds breeding in base-poor pine forests produced eggs with elevated yolk Ca concentration compared with controls, while no such effect of supplementation was detected in case of eggshell thickness. Nestling tarsus length in the first half of the nestling period was positively influenced by both yolk dry mass and yolk Ca concentration. The effect of supplementary Ca did not persist throughout the nestling period; initial effects of egg components disappeared as nestlings aged. We conclude that apparently normal eggs may harbor poor nutrient and mineral conditions for chick growth. Such subtle changes in composition of eggs can depress chick growth, especially in harsh years.     

Greater flamingos Phoenicopterus roseus are partial capital breeders

Capital breeding refers to a strategy in which birds use body stores for egg formation, whereas income breeders obtain all resources for egg formation at breeding sites. Capital breeding should occur more in large‐bodied species because the relative cost of carrying stores for egg formation becomes smaller with increasing body size. Based on a comparison between stable isotopes of carbon and nitrogen in potential prey at wintering sites and eggs, we examined whether greater flamingos use nutrients stored earlier in the year for egg production. Our results suggest that the greater flamingo is a partial income breeder, since prey for egg formation were obtained both in overwintering sites and at the breeding site. This may be because there are selective pressures for nesting females to lay soon after arriving at the breeding site, which may be facilitated by arriving at the breeding site with developed ovarian follicles.     

Lizards combine stored energy and recently acquired nutrients flexibly to fuel reproduction

1. Energy allocation strategies for reproduction are viewed typically as a continuum between reliance on 'income' (recently acquired energy) vs. 'capital' (stored reserves) for fuelling reproduction. Because ectothermy facilitates long-term energy storage and often involves low feeding rates, traditional views suggest that many ectotherms rely heavily on stored reserves for egg production. 2. We explored the temporal relationship between energy intake and expenditure in a multi-clutching lizard (Amphibolurus muricatus) by evaluating the effect of maternal nutrition on reproductive output and by contrasting delta(13)C measurements of the maternal diet and endogenous energy stores with that of the eggs produced. 3. Our experiment revealed that females utilize both endogenous energy stores and recently acquired food to fuel reproduction; this pattern did not shift seasonally from first to second clutches produced. Importantly, however, egg lipid was derived primarily from capital, whereas egg protein was derived about equally from both income and capital. 4. Overall, these results suggest that the energy allocation strategy used for reproduction differs among egg components, and that the use of recently acquired energy for reproduction may be more widespread in ectotherms than thought previously.     

Rate of nutrient allocation to egg production in a parasitic wasp

Recent years have seen a marked increase in our awareness of the need to incorporate greater physiological realism into studies of parasitoid behaviour and population dynamics. Quantification of the number of eggs produced as a result of a host-feeding event, the host-feeding gain, is essential for predicting when a parasitoid should bypass an opportunity for current reproduction (i.e. laying eggs) in order to feed from the host and, thus, increase its chances for future reproduction (i.e. producing further eggs). Using radioactively labelled amino acids, one of the main constituents of insect haemolymph, we followed the incorporation of a known quantity of nutrients into each individual egg laid over a long period of time relative to the average life span of the parasitoid. Although the maximum incorporation of nutrients obtained by the female from a discrete feeding event occurs within a short period of time, a large proportion of nutrients are stored and used gradually for egg production throughout the life of the parasitoid. We therefore provide novel experimental evidence showing that feeding gain is not a discrete event in time occurring shortly after feeding, as has so far been assumed, but is instead spread throughout the parasitoid''s lifetime. This has important consequences for calculating the increase in lifetime fitness as a result of a feeding event, a common currency of models that aim to predict feeding and oviposition behaviour in parasitoids.