Adaptations to Underground Nesting in Birds and Reptiles

Most bird eggs have evolved a suite of remarkably consistentadaptations for appropriate exchanges of respiratory gases andwater vapor during incubation in nests above ground. Howeverunderground incubation is associated with selective forces differentfrom those operating at the surface. New information from mound-buildingbirds living reptiles and extinct dinosaurs shows comergentadaptations to nest atmospheres that are high in CO₂ low inO₂ and nearly saturated with water vapor. High humidity eliminatesthe danger of excessive dehydration so gas conductance of theeggshell may be higher than normal, as a compensation for theunusual nest gases. In contrast with embryos of birds that nextabove ground and initiate breathing inside the shell, thoseof megapode birds lack an aircell and can breathe only afterthe shell is broken. Extreme precocity of megapode chicks isrelated to long incubation time and large energy stores in theegg. Because the material around a buried nest restricts diffusionthe size of the nest must be limited to prevent intolerablegas tensions adjacent to the eggs. This effect may have forcedcertain large reptiles to separate their layings into severalclutches and some megapodes to actively ventilate their mounds.     

Reassessing Breeding Investment in Birds: Class-Wide Analysis of Clutch Volume Reveals a Single Outlying Family

Reproductive investment is typically considered in terms of size and number of propagules produced. Compared with a thorough understanding of the overall patterns and ecological correlates of avian clutch size, egg size has received less attention and the total effort invested in laying a clutch of eggs is rarely considered. We used clutch volume as an alternative estimate of reproductive investment and present the first class-level analysis of clutch volume in birds using 1,364 randomly-selected species in 204 families. The relationship between body mass and egg volume was very strong (r² = 0.946), validating previous studies identifying four families (Apterygidae, Pelecanoidiididae, Sternidae and Dromadidiae) with disproportionately large eggs. Clutch volume was also closely related to body mass (r² = 0.909) and all but one of the taxa with disproportionately large eggs conformed to the overall relationship, their greater egg dimensions compensated by diminished clutch size. The only family which departed significantly from the relationship between body mass and clutch volume was the mound builders (Megapodiidae)—the only group of birds that do not rely on body heat for incubation. Although previously known for laying large clutches of large eggs containing disproportionately large yolks, the remarkable investment of megapodes in reproduction (more than seven times greater than other birds of comparable mass) has been hitherto overlooked. We consider the evolutionary basis and ecological implications of this finding, suggesting that energetic costs associated with incubation act as an upper limit on reproductive output of other birds. We recommend clutch volume as a sensitive, fine-grained measure of reproductive effort for research at a wide range of scales and advocate further analysis of ecological correlates of clutch volume in birds and amniotes generally.     

Temperature-dependent sex ratio in a bird

To our knowledge, there is, so far, no evidence that incubation temperature can affect sex ratios in birds, although this is common in reptiles. Here, we show 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, our data 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.     

Ecological,evolutionary, and conservation implications of incubation temperature‐dependent phenotypes in birds

Incubation is a vital component of reproduction and parental care in birds. Maintaining temperatures within a narrow range is necessary for embryonic development and hatching of young, and exposure to both high and low temperatures can be lethal to embryos. Although it is widely recognized that temperature is important for hatching success, little is known about how variation in incubation temperature influences the post‐hatching phenotypes of avian offspring. However, among reptiles it is well known that incubation temperature affects many phenotypic traits of offspring with implications for their future survival and reproduction. Although most birds, unlike reptiles, physically incubate their eggs, and thus behaviourally control nest temperatures, variation in temperature that influences embryonic development still occurs among nests within a population. Recent research in birds has primarily been limited to populations of megapodes and waterfowl; in each group, incubation temperature has substantial effects on hatchling phenotypic traits important for future development, survival, and reproduction. Such observations suggest that incubation temperature (and incubation behaviours of parents) is an important but underappreciated parental effect in birds and may represent a selective force instrumental in shaping avian reproductive ecology and life‐history traits. However, much more research is needed to understand how pervasive phenotypic effects of incubation temperature are among birds, the sources of variation in incubation temperature, and how effects on phenotype arise. Such insights will not only provide foundational information regarding avian evolution and ecology, but also contribute to avian conservation.     

Predation of incubator birds (Megapodius freycinet) by Komodo dragons (Varanus komodoensis)

A short study was made of the nesting habits of a species of megapode, Megapodius freycinet on the island of Komodo. The birds were found to build giant nesting mounds (0.95 × 7.15 m) in scrub and woodland close to the seashore or alongside river beds; 23 active and 19 abandoned mounds were located in an area of 250 ha.
The mounds were apparently added to from year to year, and consisted of dry sand and soil, plus leaves and sticks in most cases. The upper parts of the mounds were invariably exposed to the direct rays of the sun; the temperature within the active mounds was 33–37° C and slightly less in mounds not in use by the birds. According to the local people the nesting season of the megapodes extended from late August to November, and the chicks were hatched before the arrival of the rains in December. Up to four eggs had been recovered from a single mound.
The active mounds were all spaced apart by at least a 100 m, and the closest ones were usually separated by a river bed. This pattern suggested the species was territorial. One or two birds were often seen scraping at a mound or feeding close by, and their behaviour was recorded.
The Komodo dragon, Varanus komodoensis , was a frequent visitor to the nesting mounds of the megapodes, and was able to burrow into them and steal the eggs.     

Distribution, seasonal use, and predation of incubation mounds of Orange-footed Scrubfowl on Komodo Island, Indonesia

ABSTRACT.   Megapodes are unique in using only heat from the environment, rather than body heat, to incubate their eggs as well as the precocious independence of their chicks on hatching. Of 22 recognized species of megapodes, 9 are listed as threatened due to factors including habitat loss and fragmentation, and predation on eggs and chicks. Orange-footed Scrubfowl ( Megapodius reinwardt ) are conspicuous components of the Oriental/Austral avifauna that inhabit the monsoon forests of the Lesser Sunda chain of islands in Indonesia. We examined the abundance, patterns of distribution, physical characteristics, seasonal activity, and predation risk of incubation mounds of Orange-footed Scrubfowl on Komodo Island in eastern Indonesia. We surveyed 13 valleys on Komodo Island from April 2002 to January 2005 and located 113 tended and 107 untended incubation mounds. Densities of scrubfowl mounds in our study were similar to that reported by investigators during the 1970s, suggesting little change in the scrubfowl population since then. Most scrubfowl mounds were on sandy or loamy soils in open monsoon forest with little overhead shade, and placement of mounds in such areas may ensure adequate temperatures for egg incubation. Although some mounds were tended during all months, mound use peaked during the late wet season in March. During the dry season (April–November), only a few mounds were tended. Komodo dragons ( Varanus komodoensis ) and wild pigs ( Sus scrofa ) were the primary predators of scrubfowl eggs, with no indication of egg predation by humans. The valley with the largest number of untended mounds in our study also had the largest number of active Komodo dragon nests. This suggests an effect of Komodo dragons on scrubfowl numbers, but additional study is needed.     

Foot-mediated incubation: Nazca booby (Sula granti) feet as surrogate brood patches

Incubation in most avian species involves transferring heat from parent to egg through a highly vascularized brood patch. Some birds, however, do not develop a brood patch. Unusual among birds, these species hold their eggs under the webs of their feet, but the role of the feet in heat transfer is uncertain. Often the webs are positioned between the feathered abdomen and the egg during incubation, suggesting that either the abdomen, the feet, or both could transfer heat to the egg. We studied heat transfer from foot webs to eggs during incubation in Nazca boobies by spatially separating the feet from the abdomen using an oversized egg. We found that feet transfer heat to eggs independently of any heat that may be transferred from the abdomen. In addition, we found that incubating boobies had significantly greater vascularization in their foot webs, measured as a percentage of web area covered by vessels, than nonincubating boobies. We also found that males, whether incubating or nonincubating, had significantly less web vascularization than females. We concluded that vascularized Nazca booby feet function in the same way during incubation that vascularized brood patches do, acting as surrogate brood patches.     

Do T3 levels in incubating eiders reflect the cost of incubation among clutch sizes?

Complete development of avian eggs requires external heat, inducing in most species an energetic cost of incubation for the parents. Triiodothyronine (T(3)) has been implicated in the control of the metabolic rate and is decreased during fasting in most bird species. This raises the question of the regulation of T(3) during reproduction when incubation (thus heat production) is associated with fasting (and energy sparing). In this study, plasma concentrations of T(3) were studied for different clutch sizes in incubating, as well as in nonincubating, fasting female eiders. Our results show that the T(3) levels decrease during fasting in nonincubating birds, whereas they were maintained during the incubation fast. T(3) levels increased in female eiders at hatching. The plasma T(3) level did not vary among natural clutch sizes in eiders but did so when manipulated. T(3) levels increased when eggs were added (to a maximum of six eggs, i.e., the biggest natural clutch size) or removed (to two eggs, i.e., the smallest natural clutch size). Our results suggest that (1) high T(3) levels during incubation may participate to a threshold of heat production and incubation metabolic rate in eiders despite the fact that they are fasting; (2) since T(3) is associated with the energy expenditure in birds, incubating an enlarged or reduced clutch size may lead to a higher energetic cost of incubation in eiders; and (3) the energy demand of the ducklings at hatching is probably important, as the female T(3) concentrations are then at their highest levels. Thus, any modification of the natural clutch size leads to a rise in the T(3) level of the incubating female, suggesting an additional cost of incubation. Knowing that there is no variation of T(3) levels among natural clutch sizes, this study suggests that a female eider produces a number of eggs corresponding to the energy she can invest in incubation.     

A Large Accumulation of Avian Eggs from the Late Cretaceous of Patagonia (Argentina) Reveals a Novel Nesting Strategy in Mesozoic Birds

We report the first evidence for a nesting colony of Mesozoic birds on Gondwana: a fossil accumulation in Late Cretaceous rocks mapped and collected from within the campus of the National University of Comahue, Neuquén City, Patagonia (Argentina). Here, Cretaceous ornithothoracine birds, almost certainly Enanthiornithes, nested in an arid, shallow basinal environment among sand dunes close to an ephemeral water-course. We mapped and collected 65 complete, near-complete, and broken eggs across an area of more than 55 m². These eggs were laid either singly, or occasionally in pairs, onto a sandy substrate. All eggs were found apparently in, or close to, their original nest site; they all occur within the same bedding plane and may represent the product of a single nesting season or a short series of nesting attempts. Although there is no evidence for nesting structures, all but one of the Comahue eggs were half-buried upright in the sand with their pointed end downwards, a position that would have exposed the pole containing the air cell and precluded egg turning. This egg position is not seen in living birds, with the exception of the basal galliform megapodes who place their eggs within mounds of vegetation or burrows. This accumulation reveals a novel nesting behaviour in Mesozoic Aves that was perhaps shared with the non-avian and phylogenetically more basal troodontid theropods.     

How avian incubation behaviour influences egg surface temperatures: relationships with egg position,development and clutch size

While understanding heat exchange between incubating adults and their eggs is central to the study of avian incubation energetics, current theory based on thermal measurements from dummy eggs reveals little about the mechanisms of this heat exchange or behavioural implications for the incubating bird. For example, we know little about how birds distribute their eggs based on temperature differences among egg positions within the nest cup. We studied the great tit Parus major, a species with a large clutch size, to investigate surface cooling rates of individual eggs within the nest cup across a range of ambient temperatures in a field situation. Using state‐of‐the‐art portable infrared imaging and digital photography we tested for associations between egg surface temperature (and rate of cooling) and a combination of egg specific (mass, shape, laying order, position within clutch) and incubation specific (clutch size, ambient temperature, day of incubation) variables. Egg surface temperature and cooling rates were related to the position of the eggs within the nest cup, with outer eggs being initially colder and cooling quicker than central eggs. Between foraging bouts, females moved outer eggs significantly more than centrally positioned eggs. Our results demonstrate that females are capable of responding to individual egg temperature by moving eggs around the nest cup, and that the energy cost to the female may increase as incubation proceeds. In addition, our results showing that smaller clutches experience lower initial incubation temperatures and cool quicker than larger clutches warrant further attention for optimal clutch size theory and studies of energetic constraints during incubation. Finally, researchers using dummy eggs to record egg temperature have ignored important elements of contact‐incubation, namely the complexity of how eggs cool and how females respond to these changes.     

Effect of intermittent incubation and clutch covering on the probability of bacterial trans‐shell infection

Microbial infection is considered a critical cause of hatching failure in birds. Although several behavioural mechanisms are believed to improve reproductive success in birds, their direct effect on the risk of bacterial trans‐shell infection (BTSI) remains to be tested. Here, we focus on the protective roles of intermittent incubation and covering of the clutch with nest lining during the laying period, when eggs are highly susceptible to BTSI. To our knowledge, this study is the first to use culture‐independent PCR‐based methods to measure quantitative and qualitative indices of BTSI. In our experiment, we exposed Mallard Anas platyrhynchos eggs that were either intermittently incubated (I‐INCUB) or un‐incubated (I‐UNINCUB), and covered (COV) or uncovered (UNCOV) with nest lining. Hatchability of I‐INCUB eggs was twice that for I‐UNINCUB eggs. The presence and degree of BTSI had no effect on hatching success of experimental eggs. The residual weights of ducklings hatched from infected and I‐INCUB eggs were lower than those from uninfected and I‐UNINCUB eggs. In addition, ducklings originating from COV eggs were heavier than those hatched from UNCOV eggs. Intermittent incubation and clutch covering had no effect on the probability or degree of BTSI. Although the effect of BTSI is considered less detrimental in temperate birds, we show that the presence of BTSI inside the egg may significantly affect hatchling phenotype. This represents a novel insight into the role of BTSI in the reproductive success of birds and implies that the use of molecular PCR‐based methods is required in future studies for a better understanding of such causality.     

Physiological and Ecological Correlates of Prolonged Incubation in Sea Birds

Sea birds with long incubation periods are identified, togetherwith the features of their incubation physiology which distinguishthem from birds in general. Most sea birds with prolonged incubationare members of the order Procellariformes. The majority of Pelecaniformesand Charadniformes with long incubation periods are tropicalspecies. The total amount of water lost from the egg duringincubation is a similar fraction of the initial egg weight insea birds with prolonged incubation as in other birds. The oxygenconsumption of the newly hatched chick is similarly relatedto the chick weight, regardless of the duration of incubation.Within the constraints imposed by these similarities, sea birdswith prolonged incubation display a number of adaptations. Thedaily rate of water loss from the egg, the water vapor conductanceof the egg shell, and the total functional pore area of theegg are all relatively low in sea birds with prolonged incubation.The eggs of sea birds with long incubation times are large inrelation to the size of the adult bird in the two species thathave been studied, the high energy content of the egg is paralleledby the greater total amount of oxygen consumed during incubation.However, the growth of the embryo is relatively slow in at leastone sea bird with a long incubation time so that prolonged incubationprobably entails a comparatively high allocation of energy resourcesto maintenance requirements. In some species with prolongedincubation, the interval between pipping and hatching is alsolong and it appears to be a period of great physiological importance.Ecologically prolonged incubation is associated with eitherpelagic feeding habits or a tropical environment, both factorsmay be related to food supply.     

The role of partial incubation and egg repositioning within the clutch in hatching asynchrony and subsequent effects on breeding success

The main mechanism to achieve hatching asynchrony (HA) for incubating birds is to start heating the eggs before clutch completion. This might be achieved through partial incubation and/or early incubation. Even in the absence of incubation behaviour during the laying phase, clutches still experience a certain degree of asynchrony. Recent studies have shown that eggs located in the centre of the nest receive more heat than peripheral ones during incubation. As eggs receiving more heat would develop faster, we hypothesized that HA should be shorter in nests where eggs were moved homogeneously along the centre–periphery space during incubation than in those nests where eggs repeatedly remained in the same locations, either centrally or peripherally. We explored the relative roles of egg repositioning and partial incubation in determining HA in wild birds by (1) removing eggs from 20 Great Tit Parus major nests on the day of laying and replacing them with fake eggs to avoid partial incubation, and returning them when full incubation began; (2) monitoring twice a day the position of each individually marked egg relative to the clutch centre during incubation, and estimating the coefficient of variation of the distances; and (3) determining HA in each nest. Preventing partial incubation reduced HA by 51% days in experimental nests. It also caused negative effects for the incubating females (lengthening the full incubation period) and positive effects for the brood (increasing fledging success). However, our hypothesis about the role of egg repositioning on HA was not supported: all the females moved the eggs with remarkable consistency, generally attaining a coefficient of variation of the distances around 33%, and it was not related to the HA experienced. We therefore conclude that partial incubation is an important factor regulating HA, and females compensate for the potential effects of differential heating by moving the eggs homogeneously within the clutch.     

Effect of heat treatment on pre-stocking of Turkey eggs and its impact on incubation and hatching

Egg stocking is used to meet housing demands in the hatchery industry. Stocking periods longer than 10 days of occur commonly, despite the fact that this practice causes productive losses during the incubation process. To minimize these losses, eggs are heated before incubation to stimulate the embryo, thereby reducing the range of birth intervals. The objective of this study was to determine whether heat treatment (37.5 °C) prior to incubation would improve hatching rates. We also determined the heat-exposure time necessary to improve productivity. We stored 5376 Nicholas pedigree eggs, aged between 40 and 51 weeks, for seven days. These eggs were distributed in three groups: groups 1 and 2 received 4 and 6 h of heat treatment, respectively; group 3 was used as control (no heat treatment, remaining at 17 °C). After heat treatment, the eggs were stored for 7 days at 17 °C, together with eggs from the control group. We found significant variation in the cumulative dispersion of birds born during the hatch window; greater numbers of birds were born in group 1 that underwent the 4-h heat treatment with a 24-h hatch window and in group 3 that underwent the 6-h heat treatment with a 12-h hatch window. Hatch rate, yolk retention and the relationship between average chick weight/average egg weight did not differ between treatments. These data suggest that heat treatment modulates the hatch window; nevertheless, the treatment did not influence the average weight the chicks, the number of chicks born, the percentage of hatching or yolk retention.     

Gallilichus jonesi sp. n. (Acari: Ascouracaridae): A new species of feather mite from the quills of the Australian brush-turkey (Aves: Megapodiidae)

Adults, nymphs, larvae and eggs of Gallilichus jonesi sp. n. are described. These mites inhabit the quills of large wing and tail feathers of the megapode Alectura lathami Gray, where they appear to consume the spongy medulla inside the quill. This is the first record of Gallilichus for Australia, and the first observation of quill mites associated with the Megapodiidae. Two nymphal morphologies of G. jonesi were observed and are presumed to represent male and female, but because pharate adults were not found, definitive assignment of morphs to sexes was not possible. The only other species in the genus Gallilichus occurs in the feathers of domestic chickens. The implications of these host-associations for elucidating relationships between the megapodes and other galliform birds are discussed.     

Pelvis morphology suggests that early Mesozoic birds were too heavy to contact incubate their eggs

Numerous new fossils have driven an interest in reproduction of early birds, but direct evidence remains elusive. No Mesozoic avian eggs can be unambiguously assigned to a species, which hampers our understanding of the evolution of contact incubation, which is a defining feature of extant birds. Compared to living species, eggs of Mesozoic birds are relatively small, but whether the eggs of Mesozoic birds could actually have borne the weight of a breeding adult has not yet been investigated. We estimated maximal egg breadth for a range of Mesozoic avian taxa from the width of the pelvic canal defined by the pubic symphysis. Known elongation ratios of Mesozoic bird eggs allowed us to predict egg mass and hence the load mass an egg could endure before cracking. These values were compared to the predicted body masses of the adult birds based on skeletal remains. Based on 21 fossil species, we show that for nonornithothoracine birds body mass was 187% of the load mass of the eggs. For Enantiornithes, body mass was 127% greater than the egg load mass, but some early Cretaceous ornithuromorphs were 179% heavier than their eggs could support. Our indirect approach provides the best evidence yet that early birds could not have sat on their eggs without running the risk of causing damage. We suggest that contact incubation evolved comparatively late in birds.     

A reliable method for sexing unincubated bird eggs for studying primary sex ratio

In birds, offspring sex ratio manipulation by mothers is now well established with potentially important consequences for evolution and animal breeding. In most studies on primary sex ratio of birds, eggs are sexed after incubation by the use of PCR methods targeted to the sex-linked CHD1 genes. Sexing of unincubated eggs would be preferred, but as fertile and infertile blastodiscs cannot be distinguished macroscopically, errors could arise from PCR amplifications of parental DNA associated with the vitelline membrane of infertile eggs. In this study, we stained blastodiscs without the vitelline membrane with Hoechst 33342. This allowed unequivocal distinction between fertile and infertile blastodiscs. Fertile blastodiscs contained thousands of fluorescent nuclei, whereas no nuclei were seen in infertile eggs. In addition, after nucleic acid analysis, fertile blastodiscs yielded much stronger chromosomal DNA and CHD1-targeted PCR bands on agarose gels compared with infertile blastodiscs. These findings indicate that fertile blastodiscs contain much more embryonic DNA than parental DNA, allowing reliable sexing of the fertile eggs. The differences between fertile and infertile blastodiscs in chromosomal DNA and CHD1 PCR banding intensities alone could also be used to distinguish fertile from infertile eggs without using Hoechst staining. We conclude that identifying fertile blastodiscs either by Hoechst staining or by analyzing the yield of chromosomal DNA and CHD1-PCR products, combined with CHD1-targeted PCR amplification, presents an easy and reliable method to sex unincubated eggs.     

Clutch predation in great tinamous Tinamus major and implications for the evolution of egg color

Egg camouflage has been found to reduce predation in several ground‐nesting species. Therefore, the evolution of eggs that lack camouflage in ground nesting birds is puzzling. Even though clutch predation in the tropics is high, tinamous are the only tropical ground‐nesting birds that do not build a nest and do not lay cryptic eggs. I studied predation of great tinamou clutches in a lowland tropical forest and found that risk of predation was higher during incubation when the eggs are covered by the parent, than during laying when they are exposed, suggesting that predators primarily use cues from the incubating males to locate the clutch and not cues from the eggs. Clutch size had no effect on predation rate, even though larger clutches are more conspicuous to a human observer. Predation by visual cues is likely reduced during incubation by the camouflaged plumage and high nest attendance of males. If most predators use cues from the incubating male and not the eggs to locate clutches, then conspicuous egg color may have evolved in great tinamous as an intra‐specific signal. I evaluate hypotheses that may explain the maintenance of conspicuous egg color in tinamous.     

Do Uniparental Sanderlings Calidris alba Increase Egg Heat Input to Compensate for Low Nest Attentiveness?

Birds breeding in cold environments regularly have to interrupt incubation to forage, causing a trade-off between two mutually exclusive behaviours. Earlier studies showed that uniparental Arctic sandpipers overall spend less time incubating their eggs than biparental species, but interspecific differences in size and ecology were potential confounding factors. This study reports on a within-species comparison of breeding schedules and metal egg temperatures in uni- and biparental sanderlings (Calidris alba) in Northeast Greenland in relation to ambient temperature. We recorded incubation schedules with nest temperature loggers in 34 sanderling clutches (13 uniparentals, 21 biparentals). The temperature of a metal egg placed within the clutch of 17 incubating birds (6 uniparentals, 9 biparentals) was measured as an indicator of the heat put into eggs. Recess frequency, recess duration and total recess time were higher in uniparentals than in biparentals and positively correlated with ambient temperatures in uniparentals only. Uniparental sanderlings maintained significantly higher metal egg temperatures during incubation than biparentals (1.4°C difference on average). Our results suggest that uniparental sanderlings compensate for the lower nest attendance, which may prolong the duration of the incubation period and negatively affect the condition of the hatchlings, by maintaining a higher heat flux into the eggs.     

Are unusually colored eggs a signal to potential conspecific brood parasites?

It has previously been suggested that some species of birds make the last egg in their clutch pale as a signal to potential conspecific brood parasites that incubation has commenced. Here, we use game theory to show that the signaling function of pale eggs can be evolutionarily stable and resistant to cheating and to demonstrate that such a signal can only be maintained under strict conditions. The key conditions are, first, that there is a cost associated with the production of pale eggs (in particular, the cost of a pale egg produced early in the clutch must be more expensive than the cost of one produced later in the clutch) and, second, that the cost of making the last egg pale is not too great (relative to the costs of parasitism). We discuss the likelihood of these conditions being met in real systems and suggest empirical tests that would differentiate this theory from alternative nonadaptive explanations for pale eggs.