BIO 554/754

Avian Reproduction: Anatomy & the Bird Egg 

Photo of a hummingbird nest


Reproductive Anatomy:

Graphic showing the hypothalamus-pituitary axis
From: Akins and Burns (2001)

Graph showing changes in testosterone levels in the blood of male Song Sparrows throughout the year

The pattern of testosterone secretion in free-living populations of Song Sparrows.
Plasma levels peak in April and May as breeding got underway and then were maintained at a lower “breeding baseline” during the
rest of the breeding season. As prebasic molt ensued, plasma levels of testosterone were basal and remained so throughout autumn and winter.
From: Wingfield and Hahn (1994).

Graphic showing the multiple effects of testosterone on male birds

Biological actions of the steroid hormone testosterone. The morphological, physiological and behavioral actions of testosterone that are essential
for male reproductive function are given on the right hand and lower sides of the figure. The “costs” of prolonged high levels of testosterone are given on the
left hand side in italics. The patterns of plasma testosterone levels may be a function of secretion patterns to maintain male reproductive function, and “costs”
of testosterone that require that plasma levels be low. From Wingfield et al. (2000).

Testosterone increases availability of carotenoids -- Androgens and carotenoids play a fundamental role in the expression of secondary sex traits in animals that communicate information on individual quality. In birds, androgens regulate song, aggression, and a variety of sexual ornaments and displays, whereas carotenoids are responsible for the red, yellow, and orange colors of the integument. Parallel, but independent, research lines suggest that the evolutionary stability of each signaling system stems from tradeoffs with immune function: androgens can be immunosuppressive, and carotenoids diverted to coloration prevent their use as immunostimulants. Despite strong similarities in the patterns of sex, age and seasonal variation, social function, and proximate control, there has been little success at integrating potential links between the two signaling systems. These parallel patterns led us to hypothesize that testosterone increases the bioavailability of circulating carotenoids. To test this hypothesis, Blas et al. (2006) manipulated testosterone levels of Red-legged Partridges (Alectoris rufa) while monitoring carotenoids, color, and immune function. Testosterone treatment increased the concentration of carotenoids in plasma and liver by >20%. Plasma carotenoids were in turn responsible for individual differences in coloration and immune response. These results provide experimental evidence for a link between testosterone levels and immunoenhancing carotenoids that (i) reconciles conflicting evidence for the immunosuppressive nature of androgens, (ii) provides physiological grounds for a connection between two of the main signaling systems in animals, (iii) explains how these signaling systems can be evolutionary stable and honest, and (iv) may explain the high prevalence of sexual dimorphism in carotenoid-based coloration in animals.
Photo of a Red-legged Partridge
Red-legged Partridge (Photo by G. Bortolotti)

Sperm production

Micrograph of seminiferous tubules

Photomicrograph of sperm in a seminiferous tubule
Light photomicrograph of a section of a testis showing a seminiferous tubule during full
semen production. SG indicates spermatogonia; PS, primary spermatocyte; Ss, secondary spermatocyte;
MS, mature spermatocyte; and L, lumen (original magnification ×800) (Samour 2002).

Male birds have paired abdominal testes lying cranioventral to the first kidney lobe. Testes increase dramatically in size during the breeding season. The vas deferens emerges medially and passes caudally to the cloaca where it has a common opening with the ureter in the Urodeum. The terminal vas deferens is swollen as a storage organ: the seminal glomus (or seminal vesicle as in the drawing to the right). 

As in mammals, sperm formation is temperature sensitive, and maturation is assisted by nocturnal drops in temperature, or by the development of scrotal-like external thermoregulatory swellings holding the seminal glomera. 

In addition, male birds tend to have relatively low extragonadal sperm reserves and sperm are ejaculated soon after production in the testes.

Drawing of the reproductive system of a male bird

Photo of the cloacal protuberance of a male bird
Cloacal protuberance
Photomicrograph of a longitudinal section of the cloaca of a male Budgerigar
Longitudinal section of the cloaca of a male budgerigar during the
culmination phase of the breeding cycle. SG indicates seminal glomus;
P, proctodeum; and C, cloaca (original magnification ×12) (Samour 2002).

Drawings of the cloacal protuberance of a male Stitchbird
Cloacal protuberance of a male Stitchbird (also call the Hihi) (From: Castro et al. 1996).

Photo of the reproductive tract of a male Rock Pigeon
Photo source:

Sperm competition and testes size -- Comparative analyses suggest that a variety of ecological and behavioural factors contribute to the
tremendous variability in extrapair mating among birds. In an analysis of 1010 species of birds, Pitcher et al. (2005) examined several ecological
and behavioural factors in relation to testes size; an index of sperm competition and the extent of extrapair mating. In univariate and multivariate
analyses, testes size was significantly larger in species that breed colonially than in species that breed solitarily, suggesting that higher breeding
density is associated with greater sperm competition. After controlling for phylogenetic effects and other ecological variables, testes size was also
larger in taxa that did not participate in feeding their offspring. In analyses of both the raw species data and phylogenetically independent contrasts,
monogamous taxa had smaller testes than taxa with multiple social mates, and testes size tended to increase with clutch size, which suggests that
sperm depletion may play a role in the evolution of testes size. These results suggest that traditional ecological and behavioural variables, such as
social mating system, breeding density and male parental care can account for a significant portion of the variation in sperm competition in birds.

Testis size increases with colony size in Cliff Swallows -- By using a sample of over 800 male Cliff Swallows (Petrochelidon pyrrhonota) that died during a rare climatic event in their Nebraska study area in 1996, Brown and Brown (2003) investigated how testis size was related to body size, age, parasite load, and a bird's past colony-size history. Testis volume increased with body size. After correcting for body size, testis volume was lowest for birds age 1 and 2 years but did not vary with age for males 3 years old or more. Birds occupying parasite-free (fumigated) colonies had significantly larger testes than did birds at nonfumigated sites. Testis volume increased significantly with the size of the breeding colonies a bird had used in the past. These results show within a species that larger testes are favored in more social environments, probably reflecting a response to increased rates of extrapair copulation (and thus sperm competition) among Cliff Swallows in large colonies. The presence of ectoparasites, by inflating levels of plasma corticosterone, may in turn reduce testis mass. These data provide no support for the hypothesis that large testes, perhaps by producing more testosterone, are immunosuppressive and thus costly for that reason.
Photo of a Cliff Swallow
Photo of a breeding colony of Cliff Swallows


Photo of a Great Tit feeding nestlings
Great Tit provisioning nestlings

Temperature and the timing of reproduction -- Many bird species reproduce earlier in years with high spring temperatures, but little is known about the causal effect of temperature. Temperature may have a direct effect on timing of reproduction, but the correlation may also be indirect, for instance via food phenology. As climate change has led to substantial shifts in timing, it is essential to understand this causal relationship to predict future impacts of climate change. Visser et al. (2009) tested the direct effect of temperature on laying dates in Great Tits (Parus major) using climatized aviaries in a 6-year experiment. Temperature patterns from two specific years in which the wild population laid either early (‘warm’ treatment) or late (‘cold’ treatment) were mimicked. Laying dates were affected by temperature directly. Because the relevant temperature period started three weeks prior to the mean laying date, with a range of just 4°C between the warm and the cold treatments, and because the birds were fed ad libitum, it is likely that temperature acted as a cue rather than lifting an energetic constraint on the onset of egg production. Visser et al. (2009) also found a high correlation between the laying dates of individuals reproducing both in aviaries and in the wild, validating investigations of reproduction of wild birds in captivity. These results demonstrate that temperature has a direct effect on timing of breeding, an important step towards assessing the implication of climate change on seasonal timing.

Egg production

Avian Ovary
Photo of avian eggs
Photo of the reproductive tract of a female bird
Ovary,oviduct, & egg with shell

   In most birds, only the left ovary and oviduct persist. The ovary enlarges greatly during the breeding season. Active ovaries resemble bunches of tiny grapes -- the developing follicles. The oviduct opens medially to it in a funnel-shaped ostium. Ovulation results in the release of an egg from a mature follicle on the surface of the ovary. The egg, with extensive food reserves in the form of concentric layers of yolk, is picked up by the ostium and ciliary currents carry it into the magnum region. Over about three hours the egg receives a coating of albumen.
The egg then passes into the isthmus, where the shell membranes are deposited. This takes about one hour. The egg them moves to the uterus, or shell gland, where the calcareous shell is added and, in some birds, pigment is added in characteristic patterns. The egg then passes into the vagina and cloaca for laying.
Drawing of the reproductive tract of a female bird and how the egg forms as it moves throught the tract

Drawing showing the percentage of eggs consisting of yolk in different species of birds
Variation among bird species in the relative amount of yolk in eggs and the amount of energy available to the developing embryo (kJ-g -1, or kilojoules per gram). From top to bottom, the hatchlings are an altricial Brown Creeper, a semiprecocial Least Tern, a precocial Ruddy Duck, a superprecocial Mallee Fowl (Leipoa ocellata), and a Brown Kiwi (Apteryx australis). Kiwis are ‘outliers.’ Female kiwis produce extremely large eggs for their size (with substantial amounts of yolk), but young typically remain in the nest for several days and so are best classified as semiprecocial (From: Sotherland and Rahn 1987).

Kiwi lays an egg  

Photo of the fossilized egg of a oviraptor
The left egg found inside the female oviraptorosaurian. The
texture of the shell pieces probably resembles the original
texture of the egg. Credit: Yen-nien Cheng
Eggs discovered inside dinosaur -- The discovery of eggs inside a dinosaur has provided new clues about dinosaur reproductive biology and more support for the hypothesis that birds evolved from dinosaurs. The pair of eggs are the first found inside a dinosaur. Sato et al. (2005) found that the dinosaur produced eggs in some ways like a crocodile and in other ways like a bird. Crocodiles have two ovaries enabling them to lay a clutch of eggs. Birds have a single ovary and lay only one egg at a time. The dinosaur's egg-producing capability lay somewhere in between, suggesting a possible link with modern birds. It had two ovaries, but produce only one egg at a time from each ovary.
    Sato et al. (2005) studied a dinosaur from a group of dinosaurs called oviraptorosaurians. This type of dinosaur — probably 3 - 4 meters long — is a subgroup of the theropods. The dinosaur was excavated in China. The similar size of the eggs suggests the creature's two oviducts each produced a single egg at the same time.


Female birds can bias the sex of their chicks.-- Whether a bird is more likely to lay a male or female egg depends on which sex will have the greatest chance of doing well. Rutstein et al. (2004) adjusted the food intake of female Zebra Finches [see photo of female (left) and male (right) Zebra Finches below right] & found that well-fed females were more likely to produce daughters, while less well nourished birds were more likely to have sons. This is exactly as predicted by the fact that female offspring need to be better nourished than males if they are to survive and grow well. Photo of a pair of Zebra Finches
      The authors noted that: “In most animals sex ratio is close to 50:50 and extremely resistant to change. In mammals, including humans, the sex of the baby is determined by whether the sex chromosome in the sperm is male or female. But in birds, it is the female’s egg rather than the male’s sperm that determines what sex the chick will be. Thus the female has the potential to determine the sex of her young by whether she ovulates male or female eggs. In some way, female Zebra Finches seem to be able to exert control over whether to produce a male or female egg depending on which of the two is most likely to be successful. Our research tells us that they do it, and we understand why. The big question is: how do they do it?” 
      In many animals, females need to be well-nourished and in good condition if they are to breed, as eggs are costly to produce. Bigger eggs tend to lead to bigger young that are more likely to survive. Such ‘sex ratio adjustment’ is well documented in certain insects, such as bees and wasps, but is less well understood in birds and mammals. 
      Birds are an excellent model to use in the study of sex ratio adjustment because, using molecular techniques, scientists can establish the sex of each egg soon after laying. Further, all the resources given to the developing embryo are present in the egg at laying. Thus the size and the content of the egg are measures of the amount of resources that the female has allocated to that egg, which affects its subsequent survival chances. 
     The authors explained: “We manipulated the diet quality of Zebra Finches to look at the effects of body condition on female investment. We found that females were able to exert a strong degree of control over the production of male and female eggs. When females were fed on a low quality diet, they laid eggs that were considerably lighter than those laid when they were fed on a high quality diet, and they also laid far more male eggs on a low quality diet. This is the converse situation to that described 30 years ago for mammals, but it makes sense for Zebra Finches. Previous research has shown that under poor nutritional conditions, female Zebra Finches grow more slowly and survive less well compared to males. Therefore, females are producing more of the sex with the highest survival chances under those conditions.” 

Drawing showing two potential mechanisms for sex determination in birds
Two potential mechanisms for sex determination among birds. (A) the presence of the W chromosome triggers femaleness or (B) the presence of two Z chromosomes confers maleness.
Avian sex determination (Ellegren 2001) -- The molecular determinants behind sexual development in birds remain a mystery. The process is known to be different from that in mammals, with no homolog to the gene that confers maleness in mammals found in birds. The failure to identify such a gene in birds is probably a reflection of the fact that, despite the occurrence of two sexes being nearly universal throughout the animal kingdom, the genes involved seem virtually unrelated among metazoan phyla. These differences raise obstacles for comparative or candidate gene approaches in studies of sexual development. 
      In birds, females are the heterogametic sex, with one copy each of the Z and W sex chromosomes. Males are homogametic (ZZ). However, it is not clear whether it is the presence of the female-specific W chromosome that triggers female development, or the dose of Z chromosome that confers maleness.  An intriguing additional possibility is that both Z and W matter! In marsupials, for example, Y acts as a dominant testis determining chromosome, while the X chromosome determines the choice between pouch and scrotum. Maybe a system where the two sex chromosomes mediate different aspects of sex differentiation is also used in birds.

Graphic showing different systems of sex determination among vertebrates
Vertebrate sex determination systems. Phylogeny of major vertebrate clades showing the sex determining systems
found in members of the respective clade. ‘Multiple’ indicates involvement of more than one pair of chromosomes in sex determination.
TSD: temperature-dependent sex determination (From: Ezaz 2006).

Incubation temperature and avian sex ratios -- Although common in reptiles, incubation temperature has not been considered to be a factor in determining sex ratios Photo of a young brush turkeyin birds. However, Goth and Booth (2005) found that incubation temperature does affect sex ratios in megapodes, which are exceptional among birds because they use environmental heat sources for incubation. In the Australian Brush-turkey (Alectura lathami), a mound-building megapode, more males hatch at low incubation temperatures and more females hatch at high temperatures, whereas the proportion is 1:1 at the average temperature found in natural mounds. Chicks from lower temperatures weigh less, which probably affects offspring survival, but are not smaller. Megapodes possess heteromorphic sex chromosomes like other birds, which eliminates temperature-dependent sex determination, as described for reptiles, as the mechanism behind the skewed sex ratios at high and low temperatures. Instead, Goth and Booth (2005) suggest a sex -biased temperature-sensitive embryo mortality because mortality was greater at the lower and higher temperatures, and minimal at the middle temperature where the sex ratio was 1:1.

Copulation & fertilization:

Photo of gulls copulating

Bald Eagles mating

White-throated Kingfishers mating  

Phony phallus puts sperm ahead in bird first--  "These birds would be at it for 10-20 minutes," said co-author Tim Birkhead of the Red-billed Buffalo Weaver. Males use their organ to rub females and improve their sperm's chance of success. Few male birds have a phallus; most achieve fertilization via a cloacal kiss. So 19th-century reports of a mock member in the Buffalo Weaver sent Winterbotton et al. (2001) to Namibia. Catching the birds in the act was tough, recounts Birkhead: "In 3 years we saw eight matings." Pairs occasionally emerged from nests and flew to a nearby tree. "I'd run after them, sweating profusely with my binoculars steaming up," he says. The pair would start bouncing up and down - over numerous consecutive bouts. Compared to the 1-2 second tryst of most birds, their staying power is unique. Yet, entry of the elusive organ was hard to make out. Even in captivity "they performed beautifully," but the view was blocked, says Birkhead. So they glued a piece of cardboard to an unlucky bird's member. This did not prevent mating, suggesting that the Buffalo Weaver organ is actually a weapon in sperm wars. By choosing a male who rubs longest or best, females may be selecting top-quality sperm. Paternity testing revealed that female Buffalo Weavers sire birds from multiple males, providing evidence of sperm competition. Time spent courting must be shown to predict sperm transfer or success to really back up the idea. The 1.5-cm appendage lacks blood vessels and has a twisted furrow down its length. Males in communal nests have longer ones than those that live alone, showing that size is a factor in social success. But for males at least, the phallus is for more than foreplay.  -- Helen Pearson, Nature Science Update

Photo of a Red-billed Buffalo Weaver
Photo of the phallus of a male Red-billed Buffalo Weaver
Phalloid organ of a male buffalo weaver
(Photo source:

Drawing of the retracted and erect phallus of a male Emu or Rhea
Diagram of the left lateral view of a retracted and erect phallus of a male Emu or Rhea. The top drawing
     represents the phallus within the pouch. A. vas deferens, B. urideum, C. proctodeum, D. pocket to contain phallus,
E. erectile wall of phallus, F inverted hollow tube of phallus, G. phallic sulcus, H. erectile tissue, and I. erect phallus
with blind hollow tube.  (Source:


Four photos showing genital covariation in different species of waterfowl
Examples of genital covariation in waterfowl.

(A) Harlequin Duck (Histrionicus histrionicus) and (B) African Goose (Anser cygnoides), two species with a short phallus and no forced copulations, in which females have simple vaginas. (C) Long-tailed Duck (Clangula hyemalis), and (D) Mallard (Anas platyrhynchos), two species with a long phallus and high levels of forced copulations, in which females have very elaborate vaginas (size bars = 2 cm). ] = Phallus, * = Testis, star = Muscular base of the male phallus, > = upper and lower limits of the vagina (From: Brennan et al. 2007).

Eversion of a male Muscovy duck penis

Explosive eversion and functional morphology of the duck penis -- Coevolution of male and female genitalia in waterfowl has been hypothesized to occur through sexual conflict. This hypothesis raises questions about the functional morphology of the waterfowl penis and the mechanics of copulation in waterfowl. Brennan et al. (2010) used high-speed video of phallus eversion and histology to describe for the first time the functional morphology of the avian penis. Eversion of the 20 cm muscovy duck penis is explosive, taking an average of 0.36 sec, and achieving a maximum velocity of 1.6 m sec−1. The collagen matrix of the penis is very thin and not arranged in an axial-orthogonal array, resulting in a penis that is flexible when erect. To test the hypothesis that female genital novelties make intromission difficult during forced copulations, Brennan et al. (2010) investigated penile eversion into glass tubes that presented different mechanical challenges to eversion. Eversion occurred successfully in a straight tube and a counterclockwise spiral tube that matched the chirality of the waterfowl penis, but eversion was significantly less successful into glass tubes with a clockwise spiral or a 135° bend, which mimicked female vaginal geometry. These results support the hypothesis that duck vaginal complexity functions to exclude the penis during forced copulations, and coevolved with the waterfowl penis via antagonistic sexual conflict.

Near the junction of the vagina and shell gland of female birds are deep glands lined with simple columnar epithelium. These are the sperm storage tubules, so called because they can store sperm for long periods of time (10 days to 2 weeks). After an egg is laid, some of these sperm may move out of the tubules into the lumen of the tract, then migrate farther up to fertilize another egg.

Photomicrograph of two avian sperm
Avian sperm
Photomicrograph of avian sperm storage tubules
Avian sperm storage tubules

Photomicrographs of sperm storage tubules of domestic chickens and Wild Turkeys
Photomicrographs of sperm storage tubules contained stained and unstained spermatozoa from domestic chicken (Gallus domesticus)
hens (a, b) and turkey (Meleagris gallopavo) hens (c, d). Arrows indicate stained spermatozoa; arrowheads designate unstained spermatozoa.
Scale bars = 25 micrometers. From: King et al. (2002).

King et al. (2002) found that spermatozoa from two different inseminations (one with stained sperm, one with unstained sperm) generally
segregated into different storage tubules in both chicken and turkey hens. Storage tubules contained mixed populations of spermatozoa were
found in only 4% of chicken and 12% of turkey storage tubules examined. They concluded that the mechanism of last-male precedence does
not appear to be due to the stratification of spermatozoa within the tubules.

Photomicrograph showing innervation of sperm storage tubules

Innervation of sperm storage tubules (Freedman et al. 2001) -- Immunohistochemical staining of a turkey uterovaginal junction and sperm storage tubules. This micrograph shows a fluorescing neuron (green) near some sperm storage tubules (SST). The blue areas (se) are the surface epithelium lining the lumen of the uterovaginal junction and the epithelium of the sperm storage tubules. The arrow points to a magenta-stained area of one SST that indicates the presence of actin (a protein found in smooth muscle. The total image is 19 micrometers across.

This association between neurons and SSTs provides evidence that SSTs are innervated and suggests that the storage and release of sperm from SSTs can, perhaps, be controlled.

Post-insemination events (Birkhead and Brillard 2007) -- Most birds do not have a phallus and, in these species, insemination occurs via the so-called ‘cloacal kiss.’ Depending on taxa, sperm are ejaculated into the cloaca or vagina and rely on their motility to reach the numerous sperm-storage tubules (SSTs) located at the junction of the vagina and the uterus. As a consequence of selection during their migration through the vagina, only 1–2% of inseminated sperm enter the SSTs, the rest are probably ejected the next time that the female defecates. The SSTs contain only morphologically normal sperm, suggesting either that only normal sperm successfully traverse the vagina or that only normal sperm are ‘accepted’ by the SSTs. An unknown but probably small proportion of sperm move directly to the infundibulum (the site of fertilization) without entering the SSTs, although these are likely to fertilize only a single ovum.

That sperm in the SSTs are invariably positioned with their heads directed towards the distal end of the tubule suggests that egress from the SSTs is passive. Sperm are lost from the SSTs more or less continuously at a constant per capita rate. They enter the uterus and are carried passively to the infundibulum. Sperm accumulate or move relatively slowly through the infundibulum so that there is usually a population available to fertilize each ovum as it is ovulated. On ovulation, the ovum is captured by the prehensile, funnel-shaped infundibulum and the sperm swarm over the surface of the ovum; their target is the germinal disc, which contains the female pronucleus. At this stage, the ovum is bounded by the inner perivitelline layers (IPVL). The clustering of sperm and holes made by sperm in the IPVL around the germinal disc suggest that sperm might use chemical signals to locate the germinal disc.

In contrast to most other taxa, where only a single sperm enters the ovum, polyspermy is typical in birds. Several sperm enter the germinal disc region, hydrolyzing the IPVL via the acrosome reaction of the sperm, whereby the release of enzymes from the sperm acrosome enables the sperm nucleus to enter the ovum. However, only a single spermatozoon fuses with the female pronucleus and the remaining sperm are shifted to the periphery of the germinal disc and play no further part in development. Fertilization includes the penetration of ovum by sperm as well as the fusion of the male and female pronuclei (syngamy). Because embryo development begins almost immediately, many cell divisions have occurred by the time the ovum has become incorporated into the egg and the egg is laid (in most species) 24 hr later.

Scanning electron micrograph of a Budgerigar spermatazoon
Scanning electron photomicrograph of a 
budgerigar spermatozoon. A indicates 
acrosome; H, head; and T, tail (original 
magnification ×20000) (Samour 2002).
Transmission electron micrograph of the nucleus and midpiece of a Budgerigar spermatazoon
Transmission electron photomicrograph of the longitudinal
section of part of the nucleus and midpiece of a Budgerigar
spermatozoon. N indicates nucleus; PC, proximal centriole;
DC, distal centriole; F, axial filament complex; and
M, mitochondria (original magnification ×30000) (Samour 2002).

Fertilization of the egg usually occurs in the infundibulum.

Photomicrograph of Budgerigar sperm on the surface of a hamster ovum
Light photomicrograph of a zona-free hamster ovum with
numerous budgerigar spermatozoa bound to its surface
(original magnification ×215) (Samour 2002).

Repelling clingy exes helps snipe save sperm -- Writer Gore Vidal once said that he never passed up an opportunity to have sex or appear on television. Some male birds would disagree on at least one count. Having mated with a female, a male Great Snipe (Gallinago media) will reject her further advances and even chase her away. Male Great Snipe form leks to eye up the talent before choosing a mate. A few males get the most sex. Popular birds can get more than half of the matings, perhaps 10 a day. Hence their pickiness, suggest Saether et al. (2001). As male Great Snipe take no part in caring for their offspring, it was thought they had nothing to lose by mating as much as possible. But top males, overburdened with potential partners, must share sperm with care and spread their favors around. Sperm budgeting is the only possible explanation for male snipes' ungrateful behavior.  Like a nightclub, Great Snipe leks see their share of aggravation. "All four kinds of mating conflicts happen" - male choice, female choice, and male and female competition - explains Saether. Males are more likely to repel clingy exes if there are a lot of other females around. Females fight with one another, and males from neighboring territories chase their rivals' females away. Hostility towards old flames might be a bid to maintain order. "If a male gets rid of an unwanted female it's one less problem to worry about," says Saether. Female snipe probably seek to mate again so that they can get enough sperm to fertilize their eggs. Rejected females tend to lower their sights and settle for less popular males.  -- John Whitfield, Nature Science Update Photo of a Great Snipe
Photo by Saether et al. (2001)

The Avian Egg

Birds' eggs, like the birds themselves, vary enormously in size. The largest egg from a living bird belongs to the ostrich. It is overPhoto of the eggs of a hummingbird and an Ostrich 2000 times larger than the smallest egg produced by a hummingbird (see photo to the right; Source: Ostrich eggs are about 180 mm long and 140 mm wide and weigh 1.2 kg. Hummingbird eggs are 13 mm long and 8 mm wide and they weigh only half of a gram. The extinct Elephant Bird from Madagascar produced an egg 7 times larger than that of the Ostrich! Within the egg, three extraembryonic membranes support the life & growth of the embryo:

Drawing showing the various components of a bird egg

Drawing of a seven-day-old bird embryo

Graph showing relationship between egg mass and the duration of embryonic periods for birds in Venezuela, Argentina, and Arizona
Relative egg mass (corrected for adult mass) is greater in species with longer embryonic periods (days) among 64 passerine species in tropical Venezuela, subtropical Argentina, and north temperate Arizona. Open symbols reflect cavity-nesting species and show an interacting effect where their larger clutches are associated with relatively smaller eggs.

Egg size variation among tropical and temperate songbirds -- Species with “slow” life history strategies (long life, low fecundity) are thought to produce high-quality offspring by investing in larger, but fewer, young. Larger eggs are indeed associated with fewer eggs across taxa and can yield higher-quality offspring. Tropical passerines appear to follow theory because they commonly exhibit slow life history strategies and produce larger, but fewer, eggs compared with northern species. Martin (2008) found that relative egg mass (corrected for adult mass) varies extensively in the tropics and subtropics for the same clutch size, and proposed a hypothesis to explain egg size variation both within the tropics and between latitudes: Relative egg mass increases in species with cooler egg temperatures and longer embryonic periods to offset associated increases in energetic requirements of embryos. Egg temperatures of birds are determined by parental incubation behavior and are often cooler among tropical passerines because of reduced parental attentiveness of eggs. Cooler egg temperatures and longer embryonic periods explained the enigmatic variation in egg mass within and among regions, based on field studies in tropical Venezuela (36 species), subtropical Argentina (16 species), and north temperate Arizona (20 species). Alternative explanations were not supported. Thus, large egg sizes may reflect compensation for increased energetic requirements of cool egg temperatures and long embryonic periods that result from reduced parental attentiveness in tropical birds.

Egg composition and hatchling phenotype -- Parental investment in eggs and, consequently, in offspring can profoundly influence the phenotype, survival and evolutionary fitness of an organism. Avian eggs are excellent model systems to examine maternal allocation of energy translated through egg size variation. Dzialowski1and Sotherland (2004) used the natural range in Emu (Dromaius novaehollandiae) egg size, from 400 g to >700 g, to examine the influence of maternal investment in eggs on the morphology and physiology of hatchlings. Female Emus provisioned larger eggs with a greater absolute amount of energy, nutrients and water in the yolk and albumen. Variation in maternal investment was reflected in differences in hatchling size, which increased isometrically with egg size. Egg size also influenced the physiology of developing Emu embryos, such that late-term embryonic metabolic rate was positively correlated with egg size and embryos developing in larger eggs consumed more yolk during development. Large eggs produced hatchlings that were both heavier (yolk-free wet and dry mass) and structurally larger (tibiotarsus and culmen lengths) than hatchlings emerging from smaller eggs. As with many other precocial birds, larger hatchlings also contained more water, which was reflected in a greater blood volume. Emu maternal investment in offspring, measured by egg size and composition, is significantly correlated with the morphology and physiology of hatchlings and, in turn, may influence the success of these organisms during the first days of the juvenile stage. 
Photo of Emu chicks

Photo of an Emu egg and the skeleton of an embryo in an Emu egg
Emu egg & embryo

Drawing showing the various components of a bird egg

Yolk contains maternal antibodies -- Antibodies are deposited in eggs during yolk formation through the deposition of immunoglobulins, primarily IgY (also called IgG), in the yolk. In Chickens (Gallus domesticus), maternal IgY is catabolized by offspring over the first 14 days post-hatching and, by about 5 days post-hatching, offspring begin to synthesize their own IgY. As a result, after approximately two weeks the circulating IgY in young is principally of endogenous origin. Adult levels are attained between six weeks and six months of age. However, maternal antibodies may continue to affect offspring phenotype even after they are catabolized by influencing growth and developmental rates. In the absence of maternal IgY in chickens (due to surgical bursectomy of the mother during her own embryogenesis), the number of cells in the spleen that help lymphocytes (helper T cells) attack antigens (foreign proteins on pathogens) is depressed. Also, the immune responsiveness of offspring is depressed, which could lower the survival of offspring particularly in harsh disease environments (Grindstaff et al. 2003).
Drawing of a bird antibody
Antibodies 'attack' pathogens or toxins they produce by binding to antigens (e.g., proteins in the membranes of bacteria) via their  'binding sites' (the black areas above). This binding can neutralize toxins and attract white blood  cells that eliminate pathogens (by phagocytosis).

Graphic showing how females transfer antibodies to their eggs
Maternal secretion of antibodies and absorption by the young occur only prenatally in birds (with the exception of pigeon crop milk)
(From: Boulinier and Staszewski 2008).

Photo of a chicken egg with yellow yolk and a Black-backed Gull egg with red yolk

The familiar color of a chicken’s egg yolk (a) is in stark contrast to the richly pigmented egg yolk of a lesser Black-backed Gull, Larus fuscus (b). Such high maternal investment of carotenoids into egg yolk is typical among wild bird species, suggesting that these biologically active pigments serve important functions in the developing bird (From: Blount et al. 2000).

Why egg yolk is yellow (or red) (Blount et al. 2000) -- Egg yolk in birds is colored yellowish-red by carotenoids. Until recently, there has been no adaptive explanation of why many egg-laying animals provision their eggs so richly with carotenoids. It now appears that, in developing birds, carotenoids protect vulnerable tissues against damage caused by free radicals. Athough embryonic tissues depend on oxidizable, unsaturated fatty acids in yolk, their abundance makes the tissues susceptible to peroxidation caused by reactive oxidative metabolites and by free radicals, which are produced as normal by-products of metabolism. Protection against lipid peroxidation in young birds is afforded by the actions of yolk-derived carotenoids and other antioxidants, like vitamin E. Antioxidants also protect passively-acquired antibodies (IgY; see above) against break-down. Thus, maternal investment in egg composition, including carotenoids, might have a greater influence on offspring viability than has been realized. The use of carotenoid pigments in the sexual displays of female birds might indicate their ability to produce high quality eggs and chicks.

Photomicrograph showing keratin fibers in the outer shell membrane of an egg
Keratin fibers from the outer shell membrane can be seen above, attached to the
calcium carbonate crystals that make up the main shell structure.
Drawing showing pores in an avian eggshell

Photomicrograph of a pore in an eggshellPhotomicrograph of a pore in an eggshell
Thousands of tiny pores like the one pictured above, cover the shell, providing a passage for gas exchange.

Weaker Birds Use Steroids to Boost Offspring -- Verboven et al. (2003) reported that female gulls in poor condition were more likely to give their chicks a hormone boost to improve their chances of survival. Verboven and her colleagues experimentally enhanced maternal condition by supplementary feeding Lesser Black-backed Gulls (Larus fuscus) during egg formation and compared the concentrations of steroids (including testosterone) in their eggs with those in eggs laid by control females. Egg androgens could affect offspring performance directly through chick development and/or indirectly through changes in the competitive ability of a chick relative to its siblings. Contrary to expectation, females with experimentally enhanced body condition laid eggs with lower levels of androgens. This suggests that less healthy females pass on more steroids than healthy ones in a bid to enhance the performance of their young. Verboven noted that  “We originally thought that gulls in good condition would put more steroids in their eggs. But we discovered that healthy birds don’t tend to give their eggs the extra boost.” She compared the situation to struggling athletes who take performance-enhancing drugs. She added: “A poor sports person maybe wants to use steroids to conceal poor performance but if you are good you don’t need to use them.”
Photo of a pair of Lesser Black-backed Gulls
Lesser Black-backed Gulls
© Arthur Grosset 

Graph showing frequency of social behaviors of young gulls injected with androgens
Enhanced social behaviors (frequency h-1) and dominance in 10-month-old gulls from eggs injected with androgens
(black bars) compared to birds from eggs injected with oil (open bars). O, oblique display; F, forward display; C, charge;
P, aggressive peck; D, displacement. Sex did not affect behavior.

Avian mothers create different phenotypes by hormone deposition in their eggs -- In birds, mothers deposit substantial amounts of androgens in their eggs, and experimental evidence indicates that these maternal androgens influence the chick's early development. Despite the well-known organizing role of sex steroids on brain and behavior, studies on avian maternal egg hormones almost exclusively focus on the chick phase. Eising et al. (2005) found that, in Black-headed Gulls, maternal androgens in the egg enhance the development of the nuptial plumage and the frequency of aggressive and sexual displays (see Figure above) almost 1 year after hatching. The long-lasting effects may be mediated by an upregulation of androgen receptors later in life. Alternatively, the early hormone exposure may have influenced the hypothalamus-pituitary-gonad axis, resulting in higher androgen production later in life. The long-lasting effects of egg androgens are almost certainly beneficial for Darwinian fitness. Successful territory establishment and defense by means of aggressive interactions are essential for reproductive success in this colonial breeder. In addition, the displays are important for mate selection. Clearly, in birds, maternal hormone deposition in eggs may profoundly influence individual differentiation of fitness related traits. Since these hormones suppress early immune function of the chick and reduce long-term survival, mothers may be faced with a trade-off between producing offspring with lower survival prospects but higher reproductive success per year, or with higher chances of survival and lower annual reproductive output. By producing eggs that differ in levels of maternal hormones, mothers seem to produce a variety of phenotypes, perhaps an adaptive strategy in unpredictable environmental conditions. Since natural selection acts upon such phenotypic variation, shaping a population's demography, the role of maternal androgens in this selective process may be much greater than anticipated until now.

The Ecology of Egg Colors (see Birds: A Virtual Exhibition - The Provincial Museum of Alberta)

Egg colors and markings have strong adaptive values. Originally, birds' eggs were probably all white, as reptile eggs are. Eggs that are laid on the ground or in open nests in trees, rather than in cavities, often exhibit cryptic coloration. The eggs blend in with their surroundings and are much less visible to potential predators (e.g., a Killdeer nest).

Sometimes eggs that are laid in open nests are white at first. They then become stained by the mud and rotting vegetation in the nest. Grebes lay white eggs that become stained and cryptically colored over time.

Photo of a Red-necked Grebe nest with three eggs
Red-necked Grebe nest

In some species, such as the Common Murre, where different females lay eggs with very different markings, the uniqueness may have a purpose. Distinctive patterns, as in the eggs shown below, help females identify their own egg in a colony where thousands of eggs may dot a cliff face.

Photo showing variation in appearance of eggs of four different female Common Murres

Eggs of kingfishers and other cavity nesting birds, such as woodpeckers and some owls, are often white. The brightness of the eggs may help the parents to more easily locate them in the cavity. Shown here is the egg of a Barn Owl.

Photo of a Barn Owl egg

Photo showing variation in size and appearance of bird eggs

Evolution of egg color and patterning in birds -- Avian eggs differ so much in their color and patterning from species to species that any attempt to account for this diversity might initially seem doomed to failure. Kilner (2006) reviewed the literature that, when combined with the results of some comparative analyses, suggests that just a few selective agents can explain much of the variation in egg appearance. Ancestrally, bird eggs were probably white and immaculate. Ancient diversification in nest location, and hence in the clutch's vulnerability to attack by predators, can explain basic differences between bird families in egg appearance. The ancestral white egg has been retained by species whose nests are safe from attack by predators, while those that have moved to a more vulnerable nest site are now more likely to lay brown eggs, covered in speckles, just as Wallace hypothesized more than a century ago. Even blue eggs might be cryptic in a subset of nests built in vegetation. It is possible that some species have subsequently turned these ancient adaptations to new functions, for example to signal female quality, to protect eggs from damaging solar radiation, or to add structural strength to shells when calcium is in short supply. The threat of predation, together with the use of varying nest sites, appears to have increased the diversity of egg coloring seen among species within families, and among clutches within species. Brood parasites and their hosts have probably secondarily influenced the diversity of egg appearance. Each drives the evolution of the other's egg color and patterning, as hosts attempt to avoid exploitation by rejecting odd-looking eggs from their nests, and parasites attempt to outwit their hosts by laying eggs that will escape detection. This co-evolutionary arms race has increased variation in egg appearance both within and between species, in parasites and in hosts, sometimes resulting in the evolution of egg color polymorphisms. It has also reduced variation in egg appearance within host clutches, although the benefit thus gained by hosts is not clear.

Photo of two eggs showing greater spotting at the pointed ends

Many small songbirds have eggs with just a ‘ring’ of small spots around the broad end that does little to make the eggs cryptic. Evidence now suggests that such spots are located where the eggshell is a bit thinner (likely due to a calcium deficiency in the diet of female birds), with the pigment serving to strengthen the shell (Gosler et al. 2005). The spots consist of protoporphyrin pigment that birds synthesize during production of the heme component of hemoglobin (Burley and Vadhera 1989) and integration of this pigment into the eggshell provides additional strength. When a female bird has insufficient calcium to deposit in a shell, protoporphyrin molecules that have a semi-crystalline structure similar to that of eggshells are apparently deposited instead instead of calcium. As a result, the spots occur precisely where the shell is a bit thinner.

Photo of five eggs in an Eastern Bluebird nest

Several species of birds have blue eggs, and David Lack (1958) suggested that, in habitats where light levels are low, blue eggs might be cryptic. If true, that could help explain the blue eggs of some open-cup nesting birds that occur in forest habitats such as Wood Thrushes. However, Lack’s hypothesis cannot explain why some birds that nest in cavities, like European Starlings and Eastern Bluebirds, also have blue eggs. One hypothesis is that the blue-green color of eggshells represents a signal of female quality to their mates ( Moreno and Osorno 2003). The pigment responsible for the blue-green color is biliverdin, a substance produced when the hemoglobin of damaged red blood cells is catabolized and also known to have strong antioxidant properties. Antioxidants are important because they can convert free radicals, molecules that can damage DNA, proteins, and other macromolecules, into less reactive substances. Deposition of this pigment in eggshells by laying females may, therefore, signal their capacity to produce antioxidants and control free radicals. Male birds paired to females of such quality that they are able to deposit antioxidants in eggshells rather than retaining them may then expend greater effort in caring for their superior offspring (Kilner 2006). In support of this hypothesis, the provisioning rates of male Pied Flycatchers (Ficedula hypoleuca) and the intensity of the blue coloration of eggs were found to be positively correlated (Moreno et al. 2004). Also, female Eastern Bluebirds in better body condition were found to lay more colorful eggs, supporting the hypothesis that biliverdin pigmentation in eggshells reflects female condition (Siefferman et al. 2006).


"Initially the female stood motionless in the nest cup. The first sign of approaching egg- laying was usually intensified breathing, occasionally with rhythmic opening and closing of the bill that pointed either horizontally forwards or more or less upwards. The head was drawn in and the body feathers were somewhat fluffed out; the Coal Tit in addition raised its crown feathers. The tail was kept horizontal or elevated up to about 45 degrees”. Then the tip of the tail started nodding movements synchronously with rhythmic depressions of the rump.These movements which apparently were caused by throes of parturition when the egg traveled down the oviduct, were almost invisible to begin with but gathered in strength and ended with a sudden elevation of the rump that marked the moment of egg-laying. Then the bird “froze” in a motionless posture, termed “recovery phase.” This last rise of the rump clearly indicated that the egg had just been laid.

Duration of egg-laying varies a great deal even within species. The opening and closing of the bill and rhythmic movements of the back and tip of the tail occurs repeatedly for up to 4 minutes in the Prairie Warbler, presumably corresponding to the duration of egg- laying. For 3 eggs of the Goldcrest, only 8-9 seconds elapsed between the first visible sign of pressure and the moment of egg- laying. In tits, this period varied from about 10 to 77 seconds, mostlv 20-30 seconds. The Cuckoo (Cuculus canorth) which is a brood parasite, is known to lay the egg remarkably swift, usually within 10 seconds with a lower limit of only 3-4 seconds. Presumably this short duration is an adaptation to its parasitic behavior."--- From: Haftorn (1996).

X-ray of a female Kiwi with an egg in its oviduct

Drawing showing how an egg in ejected from the cloaca

Photo showing an egg being laid

Female birds turns part of the cloaca and the last segment of the oviduct inside out ("like a glove"). The vent is then everted and the egg emerges far outside at the end of the bulge. As a result, the egg does not contact the walls of the cloaca and get contaminated by feces. In addition, the intestine and inner part of the cloaca are kept shut by the emerging egg, and their contents cannot leave when the hen strains to deliver the egg. Therefore, eggs are always clean when laid (van der Molen 2002).

Wandering Albatross laying an egg

Kiwi laying an egg

Literature Cited:

Akins, C. & M. Burns. 2001. Visual control of sexual behavior. In R. G. Cook  (Ed.), Avian visual cognition [On-line]. Available:

Birkhead, T. R. and J.-P. Brillard. 2007. Reproductive isolation in birds: postcopulatory prezygotic barriers. Trends in Ecology and Evolution 22: in press.

Blas, J., L. Perez-Rodriguez, G. R. Bortolotti, J. Vinuela, and T. A. Marchant. 2006. Testosterone increases bioavailability of carotenoids: insights into the honesty of sexual signaling. Proceedings National Academy of Sciences 103: 18633-18637.

Blount, J. D., D. C. Houston, and A. P. Møller. 2000. Why egg yolk is yellow. Trends in Ecology and Evolution 15: 47-49.

Boulinier, H. and V. Staszewski. 2008. Maternal transfer of antibodies: raising immuno-ecology issues. Trends in Ecology and Evolution, in press.

Brennan, P. L. R., C. J. Clark, and R. O. Prum. 2010. Explosive eversion and functional morphology of the duck penis supports sexual conflict in waterfowl genitalia. Proceedings of the Royal Society B, online early.

Brennan, P. L., R. O. Prum, K. G. McCracken, M. D. Sorenson, R. E. Wilson, and T. R. Birkhead. 2007. Coevolution of male and female genital morphology in waterfowl. PLoS ONE 2: e418.

Brown, C.R. and M. B. Brown. 2003. Testis size increases with colony size in cliff swallows. Behavioral Ecology 14:569-575.

Burley, R. W. and D. V. Vadhera. 1989. The avian egg. John Wiley, New York, NY.

Castro, I., E. O. Minot, R. A. Fordham, and T. R. Birkhead. 1996. Polygynandry, face-to-face copulation and sperm competition in the Hihi Notiomystis cincta (Aves: Meliphagidae). Ibis 138: 765-771.

Dzialowskil, E. M. and P. R. Sotherland. 2004. Maternal effects of egg size on emu Dromaius novaehollandiae egg composition and hatchling phenotype. J. Exp. Biol. 207:597-606.

Eising, C. M., W. Müller & T. G.G. Groothuis. 2005. Avian mothers create different phenotypes by hormone deposition in their eggs. Proc. Royal Soc. London, Biol. Letters: early on-line.

Ellegren, H. 2001. Hens, cocks and avian sex determination: a quest for genes on Z or W? European Molecular Biology Organization Reports 2:192-196.

Ezaz, T., R. Stiglec, F. Veyrunes, and J. A. Marshall Graves. 2006. Relationships between Vertebrate ZW and XY Sex Chromosome Systems. Current Biology 16: R736-R743.

Freedman, S. L., V. G. Akuffo, and M. R. Bakst. 2001. Evidence for the innervation of sperm storage tubules in the oviduct of the turkey (Meleagris gallopavo). Reproduction 121: 809-814.

Gosler, A.G., J. P. Higham, and S. J. Reynolds. 2005. Why are birds’ eggs speckled? Ecology Letters 8: 1105-1113.

Goth, A. and D. T. Booth. 2005. Temperature-dependent sex ratio in a bird. Biology Letters 1: 31-33.

Grindstaff, J. L., E. D. Brodie III, and E. D. Ketterson. 2003. Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc. Royal Soc. Lond. B 270: 2309-2319.

Kilner, R. M. 2006. The evolution of egg colour and patterning in birds. Biological Reviews 81: 383–406.

Haftorn, S. 1996. Egg-laying behavior in tits. Condor 98:863-865.

King, L.M., J. P. Brillard, W.M. Garrett, M.R. Bakst, and A.M. Donoghue. 2002. Segregation of spermatozoa within sperm storage tubules of fowl and turkey hens. Reproduction 123:79-86.

Lack, D. 1958. The significance of the colour of turdine eggs. Ibis 100: 145-166.

Martin, T. E. 2008. Egg size variation among tropical and temperate songbirds: an embryonic temperature hypothesis. Proceedings of the National Academy of Sciences USA 105: 9268-9271.

Moreno, J. and J. L. Osorno. 2003. Avian egg color and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? Ecology Letters 6: 803-806.

Moreno, J., J. L. Osorno, J. Morales, S. Merino, and G. Tomás. 2004. Egg coloration and male parental effort in the Pied Flycatcher Ficedula hypoleuca. Journal of Avian Biology 35:300–304.

Pettingill, O.S., Jr. 1985. Ornithology in Laboratory and Field, Fifth ed. Academic Press, New York, NY.

Pitcher, T. E., P. O. Dunn & L. A. Whittingham. 2005. Sperm competition and the evolution of testes size in birds. Journal of Evolutionary Biology 18: 557-567.

Rosenzweig, M.R., A.L. Leiman and S.M. Breedlove. 1996. Biological Psychology. Sinauer Associates, Sunderland, MA.

Rutstein, A.N.,  P. J. B. Slater, and  J. A. Graves. 2004. Diet quality and resource allocation in the zebra finch. Proc. R. Soc. Lond.  B (Suppl.). Published online, 20 February 2004.

Saether, S. A., P. Fiske, & J. A. Kalas. 2001. Male mate choice, sexual conflict and strategic allocation of copulations in a lekking bird. Proceedings of the Royal Society London B 268: 2097 - 2102.

Samour, Jaime H. 2002. The Reproductive Biology of the Budgerigar (Melopsittacus undulatus): Semen Preservation Techniques and Artificial Insemination Procedures. Journal of Avian Medicine and Surgery 16: 39-49.

Sato, T., Yen-nien Cheng, Xiao-chun Wu, D. K. Zelenitsky, & Yu-fu Hsiao. 2005. A Pair of Shelled Eggs Inside A Female Dinosaur. Science 308:375.

Siefferman, L., K. J. Navara, and G. E. Hill. 2006. Egg coloration is correlated with female condition in Eastern Bluebirds (Sialia sialis). Behavioral Ecology and Sociobiology 59: 651-656.

Sotherland, P. R. and H. Rahn. 1987. On the composition of bird eggs. Condor 89: 48-65.

van der Molen, W. H. 2002. Laying an egg.

Verboven, N., P. Monaghan, D.M. Evans, H. Schwabl, N. Evans, C. Whitelaw, and R.G. Nager. 2003. Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the Lesser Black-backed Gull (Larus fuscus). Proceedings of the Royal Society: Biological Sciences 270: 2223 - 2232

Visser, M. E., L. J. M. Holleman, and S. P. Caro. 2009. Temperature has a causal effect on avian timing of reproduction. Proceedings of the Royal Society B: online early.

Welty, J.C. and L. Baptista. 1988. The life of birds, fourth ed. Saunders College Publishing, New York, NY.

Wingfield, J. C., and T. P. Hahn. 1994. Testosterone and territorial behaviour in sedentary and migratory sparrows: Animal Behaviour 47: 77–89.

Wingfield, J. C., J. D. Jacobs, A. D. Tramontin, N. Perfito, S. Meddle, D. L. Maney, and K. Soma. 2000. Toward and ecological basis of hormone-behavior interactions in reproduction of birds: In K. Wallen and J. Schneider (eds.), Reproduction in context, pp. 85–128. MIT Press, Cambridge.

Winterbotton, M., T. Burke, & T. R. Birkhead. 2001. The phalloid organ, orgasm and sperm competition in a polygandrous bird: the red-billed buffalo weaver. Behavioural Ecology and Sociobiology 50: 474-482.

Back to BIO 554/754 Syllabus

Back to Avian Biology