Measuring temporal variation in reproductive output reveals optimal resource allocation to reproduction in the northern grass lizard, Takydromus septentrionalis

We measured the reproductive output of Takydromus septentrionalis collected over 5 years between 1997 and 2005 to test the hypothesis that reproductive females should allocate an optimal fraction of accessible resources in a particular clutch and to individual eggs. Females laid 1–7 clutches per breeding season, with large females producing more, as well as larger clutches, than did small females. Clutch size, clutch mass, annual fecundity, and annual reproductive output were all positively related to female size (snout–vent length). Females switched from producing more, but smaller eggs in the first clutch to fewer, but larger eggs in the subsequent clutches. The mass-specific clutch mass was greater in the first clutch than in the subsequent clutches, but it did not differ among the subsequent clutches. Post-oviposition body mass, clutch size, and egg size showed differing degrees of annual variation, but clutch mass of either the first or the second clutch remained unchanged across the sampling years. The regression line describing the size–number trade-off was higher in the subsequent clutch than in the first clutch, but neither the line for first clutch, nor the line for the second clutch varied among years. Reproduction retarded growth more markedly in small females than in large ones. Our data show that: (1) trade-offs between size and number of eggs and between reproduction and growth (and thus, future reproduction) are evident in T. septentrionalis ; (2) females allocate an optimal fraction of accessible resources in current reproduction and to individual eggs; and (3) seasonal shifts in reproductive output and egg size are determined ultimately by natural selection.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 315–324.     

Clutch size variation in the Nazca booby: a test of the egg quality hypothesis

In obligately siblicidal bird species, aggressive behavior bya dominant chick results in a fixed brood size of one, yetthese species usually show clutch size variation between individuals.Simmons proposed that variation in clutch size in obligatelysiblicidal species is related to a trade-off between egg qualityand egg quantity: some individuals produce a single highly hatchable egg, while others produce two small, lower qualityeggs. We tested the egg quality hypothesis as an explanationfor observed clutch size variation in the Nazca booby (Sulagranti), an obligately siblicidal seabird. We tested the assumptionthat egg volume is positively correlated with hatchabilityand the prediction that eggs from one-egg clutches are largerthan eggs from two-egg clutches. We did not find a positive relationship between egg volume and hatchability in this species.Eggs from two-egg clutches were either equivalent in volumeor larger than eggs from one-egg clutches. Thus, the egg qualityhypothesis was rejected as an explanation for clutch size variationin the Nazca booby. Instead, two-egg clutches appear to befavored because of the insurance value of the second-laid egg,while one-egg clutches result from food limitation.     

Does the cost of incubation set limits to clutch size in common eiders Somateria mollissima?

We examined the effect of natural clutch size on the cost of incubation in a population of common eiders Somateria mollissima nesting in Tromsø, northern Norway. The body condition of females at day 5 in the incubation period was not related to clutch size (3–6 eggs), but females incubating large clutches lost more mass and had a lower body condition at day 20 in the incubation period than females incubating small clutches. Females incubating large clutches had a slightly shorter incubation period and a lower egg predation rate. The results do not support the hypothesis that the female's ability to produce eggs is the only ultimate control of clutch size in eider. Instead the results suggest that there may be an interaction between the allocation of body reserves to eggs and incubation, and that females producing large clutches allocate more of their body reserves to incubation than females producing small clutches, in order to shorten the incubation period and to minimise the risk of predation on eggs.     

Annual variation in the seasonal shift in egg size and clutch size in Sceloporus woodi

Summary Early and late season clutch parameters were examined over a three year period in the Florida scrub lizard, Sceloporus woodi. Precipitation levels were monitored throughout the study. In the early and late season of 1984 and the early season of 1986 precipitation levels approximated long-term mean levels of precipitation. In 1985 a severe winter drought occurred. Clutch size was positively related to body size in all samples in every year. In 1984 and 1986, egg size was not related to clutch size, whereas, in 1985 egg size was negatively related to clutch size. In 1985, females produced large clutches of small eggs early in the season and small clutches of large eggs late in the season. In 1984, no seasonal changes in egg or clutch size occurred. In the late season of 1986, females produced the largest clutches and the smallest eggs of all the samples, but egg and clutch size were not statistically different from the early season egg and clutch size of 1986. Total clutch dry weight, an estimate of total clutch energy, was not different in any of the six sampling periods. These data do not support current adaptationist models that attempt to explain the control of clutch and egg size in lizards. It is argued in this paper that egg and clutch size may vary in response to past environments that affect a female's physical condition, as well as, current resources that may be important for maintenance and reproduction. Egg and clutch size appear to be plastic traits selected to respond to proximal environmental variation, whereas, the investment of total dry matter/clutch has been optimized.     

Egg-size variation in the bluethroat (Luscinia s. svecica): constraints and adaptation

We examined inter- and intra-clutch egg-size variation in the bluethroat (Luscinia s. svecica), an open-nesting passerine breeding in the sub-alpine region in southern Norway. By removing first clutches shortly after egg-laying, we induced laying of a repeat clutch. Females significantly reduced the number of eggs from the first to the second nesting attempt, but increased mean egg size. Females in good condition laid significantly larger eggs than those in poor condition. Consistent with predictions of the brood survival hypothesis, assuming an adaptive investment in last eggs to ensure survival of all eggs in the clutch, we found that the size of the last eggs in first clutches was generally larger than the mean egg size of the clutch, and that the relative size of the last egg increased with clutch size. However, a large last egg reflected a general increase in egg size throughout the laying sequence rather than a specific investment in the last egg only. Egg size was not significantly influenced by sex or paternity (within-pair versus extra-pair) of the embryo. In repeat clutches the last egg was not consistently larger than the mean for the clutch. We conclude that female bluethroats face resource limitations during egg formation early in the season, and that the patterns of increase in egg size with laying order for first clutches, and from first to repeat clutches, can largely be explained by proximate constraints on egg formation.     

Influence of egg size differences within egg clutches on larval parameters in nine libellulid species (Odonata)

Abstract.  1. In libellulids, egg size differs between species and populations. There are also size differences within egg clutches of individual females.
2. Past experiments suggest that there are two different types of egg clutches in libellulids. Egg size decreases significantly during oviposition in species that perform non-contact guarding during oviposition. In contrast, in species ovipositing in tandem, egg size is randomly distributed.
3. This study deals with the possible consequences of egg size variation within the different egg clutch types. The study examined whether there is a correlation between egg development time, offspring sex or larval size and egg size.
4. The current experiments were conducted in Namibia and Germany. Five non-contact guarding and four tandem guarding libellulid species were used.
5. In some species larger eggs needed more time to develop, in some species no correlation between egg size and egg development time could be found, whereas in other species larger eggs developed faster.
6. The sex ratio was biased towards females in Leucorrhinia dubia and in Sympetrum striolatum and egg size was not associated with gender.
7. In both egg clutch types larger eggs resulted in larger larvae. In this study, evidence was found that the effects of egg size diminished with progressing larval development under good conditions. However, it is possible that the effects may have a greater influence under harsh circumstances.     

Clutch size manipulation, hatching success and offspring phenotype in the ball python (Python regius)

In a diverse array of avian and mammalian species, experimental manipulations of clutch size have tested the hypothesis that natural selection should adjust numbers of neonates produced so as to maximize the number of viable offspring at the end of the period of parental care. Reptiles have not been studied in this respect, probably because they rarely display parental care. However, females of all python species brood their eggs until hatching, but they do not care for their neonates. This feature provides a straightforward way to experimentally increase or reduce clutch size to see whether the mean clutch size observed in nature does indeed maximize hatching success and/or optimize offspring phenotypes. Eggs were removed or added to newly laid clutches of Ball Pythons ( Python regius ) in tropical Africa (nine control clutches, eight with 50% more eggs added, six with 42% of eggs removed). All clutches were brooded by females throughout the 2-month incubation period. Experimental manipulation of clutch-size did not significantly affect the phenotypes (morphology, locomotor ability) of hatchlings, but eggs in 'enlarged' clutches hatched later, and embryos were more likely to die before hatching. This mortality was due to desiccation of the eggs, with females being unable to cover 'enlarged' clutches sufficiently to retard water loss. Our results support the notion of an optimal clutch size, driven by limitations on parental ability to care for the offspring. However, the proximate mechanisms that generate this optimum value differ from those previously described in other kinds of animals. © 2003 The Linnean Society of London . Biological Journal of the Linnean Society 2003, 78 , 263–272.     

A comparative study of egg mass and clutch size in the Anseriformes

The factors explaining interspecific differences in clutch investment in precocial birds are poorly understood. We investigated how variations in clutch characteristics are related to environmental factors in a comparative study of 151 extant species of ducks, geese and swans (Anseriformes). Egg mass was negatively related to clutch size in a phylogenetic regression, a relationship that was much stronger when controlling for female mass. Nest placement was related to both egg size and clutch size, with cavity-nesting species laying more but smaller eggs. Egg size was positively correlated with incubation period and with female mass, and also with sexual size dimorphism (i.e. male mass relative to that of the female). Clutch size was not related to female mass. Species with long term pair bonds laid smaller clutches and larger eggs. The size of the breeding range was strongly positively correlated with clutch size and clutch mass, and its inclusion in multivariate models made other biogeographical variables (hemisphere, breeding latitude or insularity) non-significant. The small clutches in insular species appear to be a product of small range size rather than insularity per se. Our results suggest there is an evolutionary trade-off between clutch and egg size, and lend support to Lack’s resource-limitation hypothesis for the waterfowl.     

Incubation capacity contributes to constraints on maximal clutch size in Brent Geese Branta bernicla nigricans

Lack ( 1967 ) proposed that clutch size in species with precocial young was determined by nutrients available to females at the time of egg formation; since then others have suggested that regulation of clutch size in these species may be more complex. We tested whether incubation limitation contributes to ultimate constraints on maximal clutch size in Black Brent Geese (Black Brant) Branta bernicla nigricans. Specifically, we investigated the relationship between clutch size and duration of the nesting period (i.e. days between nest initiation and the first pipped egg) and the number of goslings leaving the nest. We used experimental clutch manipulations to assess these questions because they allowed us to create clutches that were larger than the typical maximum of five eggs in this species. We found that the per‐capita probability of egg success (i.e. the probability an egg hatched and the gosling left the nest) declined from 0.81 for two‐egg clutches to 0.50 for seven‐egg clutches. As a result of declining egg success, clutches containing more than five eggs produced, at best, only marginally more offspring. Manipulating clutch size at the beginning of incubation had no effect on the duration of the nesting period, but the nesting period increased with the number of eggs a female laid naturally prior to manipulation, from 25.4 days (95% CI 25.1–25.7) for three‐egg clutches to 27.7 days (95% CI 27.3–28.1) for six‐egg clutches. This delay in hatching may result in reduced gosling growth rates due to declining forage quality during the brood rearing period. Our results suggest that the strong right truncation of Brent clutches, which results in few clutches greater than five, is partially explained by the declining incubation capacity of females as clutch size increases and a delay in hatching with each additional egg laid. As a result, females laying clutches with more than five eggs would typically gain little fitness benefit above that associated with a five‐egg clutch.     

Body-size effect on egg size in eublepharid geckos (Squamata: Eublepharidae), lizards with invariant clutch size: negative allometry for egg size in ectotherms is not universal

Within a single clutch, smaller species of ectotherms generally lay a smaller number of relatively larger eggs than do larger species. Many hypotheses explaining both the interspecific negative allometry in egg size and egg size–number trade-off postulate the existence of an upper limit to the egg size of larger species. Specifically, in lizards, large eggs of large species could have too long a duration of incubation, or they could be too large to pass through the pelvic opening, which is presumably constrained mechanically in larger species. Alternatively, negative allometry could be a result of limits affecting eggs of smaller species. Under the latter concept, hatchling size in smaller species may be close to the lower limit imposed by ecological interactions or physiological processes, and therefore smaller species have to invest in relatively larger offspring. Contrary to these lower limit hypotheses, explanations based on the existence of an upper limit always predict negative egg-size allometry even in animals with invariant clutch size, in which naturally there is no egg size–number trade-off. We studied egg-size allometry in lizards of the family Eublepharidae, a monophyletic group of primitive geckos with large variance in body size and an invariant number of two eggs per clutch. We found an isometric relationship between egg and female size that does not support the upper limit hypotheses.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 527–532.     

Offspring size and survival in the frog Rana latastei: from among-population to within-clutch variation

Egg size is considered to be a major maternal effect for offspring in oviparous organisms. It has profound consequences on fitness, and differences in egg size are viewed as plastic responses to environmental variability. However, it is difficult to identify the effect of egg size per se because egg size can covary with genetic features of the mother and with other nongenetic factors. We analysed the relationship between offspring starting size (i.e. a proxy of egg size) and larval survival in the frog Rana latastei . We analysed this relationship: (1) among five populations at different altitudes; (2) among clutches laid from different females; and (3) among siblings within clutches, to evaluate the effect of starting size. We observed differences among populations for offspring size, but starting size was not related to altitude or genetic diversity. Mortality was higher in populations and families with small average starting size; however, among siblings, the relationship between starting size and mortality was not verified. The relationship observed among clutches may therefore be caused by covariation between egg size and other effects. This suggests that the covariation between egg size and other effects can result in apparent relationships between egg size and fitness-related traits. Proximate and ultimate factors can cause the phenotypic variation of hatchlings in the wild, and key traits can be related to this variation, but the underlying causes require further investigation.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 845–853.     

Female reproductive characteristics of the Balkan wall lizard (<Emphasis Type="Italic">Podarcis taurica</Emphasis>) in the northwestern periphery of its range

We present data on the female reproductive traits of the Balkan wall lizard in the Deliblato Sand, a large continental sandland in the Pannonian area in the northwestern periphery of the species range. The clutch and egg characteristics of the population were investigated on the basis of clutches laid in laboratory conditions by gravid females captured in one locality. Balkan wall lizards produced at least two clutches in a breeding season. Individual females laid clutches of commonly two (range 1–4) eggs. The female body size had no effect on clutch and egg size. There was no trade-off between egg size and clutch size.     

Maternal investment in reproduction and its consequences in leatherback turtles

Maternal investment in reproduction by oviparous non-avian reptiles is usually limited to pre-ovipositional allocations to the number and size of eggs and clutches, thus making these species good subjects for testing hypotheses of reproductive optimality models. Because leatherback turtles (Dermochelys coriacea) stand out among oviparous amniotes by having the highest clutch frequency and producing the largest mass of eggs per reproductive season, we quantified maternal investment of 146 female leatherbacks over four nesting seasons (2001–2004) and found high inter- and intra-female variation in several reproductive characteristics. Estimated clutch frequency [coefficient of variation (CV) = 31%] and clutch size (CV = 26%) varied more among females than did egg mass (CV = 9%) and hatchling mass (CV = 7%). Moreover, clutch size had an approximately threefold higher effect on clutch mass than did egg mass. These results generally support predictions of reproductive optimality models in which species that lay several, large clutches per reproductive season should exhibit low variation in egg size and instead maximize egg number (clutch frequency and/or size). The number of hatchlings emerging per nest was positively correlated with clutch size, but fraction of eggs in a clutch yielding hatchlings (emergence success) was not correlated with clutch size and varied highly among females. In addition, seasonal fecundity and seasonal hatchling production increased with the frequency and the size of clutches (in order of effect size). Our results demonstrate that female leatherbacks exhibit high phenotypic variation in reproductive traits, possibly in response to environmental variability and/or resulting from genotypic variability within the population. Furthermore, high seasonal and lifetime fecundity of leatherbacks probably reflect compensation for high and unpredictable mortality during early life history stages in this species.     

Geographical variation in reproductive traits and trade‐offs between size and number of eggs in the king ratsnake,Elaphe carinata

We collected gravid king ratsnakes (Elaphe carinata) from three geographically separated populations in Chenzhou (CZ), Lishui (LS) and Dinghai (DH) of China to study the geographical variation in female reproductive traits and trade‐offs between the size and number of eggs. Not all reproductive traits varied among the three populations. Of the traits examined, five (egg‐laying date, post‐oviposition body mass, clutch size, egg mass and egg width) differed among the three populations. The egg‐laying date, ranging from late June to early August, varied among populations in a geographically continuous trend, with females at the most northern latitude (DH) laying eggs latest, and females at the most southern latitude (CZ) laying eggs earliest. Such a trend was less evident or even absent in the other traits that differed among the three populations. CZ and DH females, although separated by a distance of approximately 1100 km as the crow flies, were similar to each other in most traits examined. LS females were distinguished from CZ and DH females by the fact that they laid a greater number of eggs, but these were smaller. The egg size–number trade‐off was evident in each of the three populations and, at a given level of relative fecundity, egg mass was significantly greater in the DH population than in the LS population. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 701–709.     

Different Temperature and Cooling Patterns at the Blunt and Sharp Egg Poles Reflect the Arrangement of Eggs in an Avian Clutch

Incubation is an energetically demanding process during which birds apply heat to their eggs to ensure embryonic development. Parent behaviours such as egg turning and exchanging the outer and central eggs in the nest cup affect the amount of heat lost to the environment from individual eggs. Little is known, however, about whether and how egg surface temperature and cooling rates vary among the different areas of an egg and how the arrangement of eggs within the clutch influences heat loss. We performed laboratory (using Japanese quail eggs) and field (with northern lapwing eggs) experiments using infrared imaging to assess the temperature and cooling patterns of heated eggs and clutches. We found that (i) the sharp poles of individual quail eggs warmed to a higher egg surface temperature than did the blunt poles, resulting in faster cooling at the sharp poles compared to the blunt poles; (ii) both quail and lapwing clutches with the sharp poles oriented towards the clutch centre (arranged clutches) maintained higher temperatures over the central part of the clutch than occurred in those clutches where most of the sharp egg poles were oriented towards the exterior (scattered clutches); and (iii) the arranged clutches of both quail and lapwing showed slower cooling rates at both the inner and outer clutch positions than did the respective parts of scattered clutches. Our results demonstrate that egg surface temperature and cooling rates differ between the sharp and blunt poles of the egg and that the orientation of individual eggs within the nest cup can significantly affect cooling of the clutch as a whole. We suggest that birds can arrange their eggs within the nest cup to optimise thermoregulation of the clutch.     

Geographic variation in reproductive traits and trade-offs between size and number of eggs of the Chinese cobra (Naja atra)

We collected gravid Chinese cobras (Naja atra) from one island (Dinghai) and three mainland (Yiwu, Lishui and Quanzhou) populations in south‐eastern China to study geographical variation in female reproductive traits and the trade‐off between the size and number of eggs. We then conducted an common experiment on cobras from two of the four populations to further identify factors contributing to the observed trade‐offs. The mean size (snout–vent length) of the smallest five reproductive females increased with increasing latitude. Oviposition occurred between late June and early August, with females from the warmer localities laying eggs earlier than those from the colder localities. Maternal size was a major determinant of the reproductive investment in all populations, with larger females producing not only more but also larger eggs. Clutch size was more variable than egg size within and among populations. The observed geographical variation in clutch size, egg size, clutch mass and post‐oviposition body condition was not a simple consequence of variation in maternal size among populations, because interpopulation differences in these traits were still evident when the influence of maternal size was removed. The upper limit to reproductive investment was more likely to be set by the space availability in the island population, but by the resource availability in the three mainland populations. Trade‐offs between size and number of eggs were detected in all populations, with females that had larger clutches for their size having smaller eggs. Egg size at any given level of relative fecundity differed among populations, primarily because of interpopulation differences in the resource availability rather than the space availability. Except for the timing date of oviposition and the mean size of the smallest five reproductive females, all other examined traits did not vary in a geographically continuous trend. The common garden experiment, which standardized environmental factors, synchronized the timing date of oviposition, but it did not modify the conclusion drawn from the gravid females collected from the field. The observed geographical variation in the female reproductive traits could be attributed to the consequence of the effects of either proximate or ultimate factors. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85 , 27–40.     

Relationship between clutch size,egg volume and hatching success in a Yellow-legged Gull Larus michahellis colony in south-eastern Tunisia

This study aimed to test the hypothesis that clutch size covaries with egg volume and hatching success in the Yellow-legged Gull Larus michahellis. We determined clutch size and egg volume in a sample of 131 nests, and we used the data to check whether egg volume varied among nests according to clutch size, while taking into account the effects of egg laying order. We also estimated hatching success rate and investigated the relationship between hatching success and clutch size. Egg volume varied among clutches according to clutch size, with eggs being larger in three-egg clutches than in two-egg clutches. Moreover, three-egg clutches showed higher daily survival rates, and hence hatching success, than two-egg clutches. Overall, our results suggest that in the Yellow-legged Gull clutch size covaries with egg volume and hatching success, which could possibly reflect an age effect through different mechanisms. Indeed, older females could be hypothesised to exhibit greater breeding performance than younger females because of their higher experience in tapping energy resources for egg formation and defending nests from dangers. Moreover, due to their age, older females are likely to have lower residual reproductive potential and should invest more heavily in current breeding attempts.     

Experimental demonstration of the insurance value of extra eggs in an obligately siblicidal seabird

A variety of organisms regularly produce more offspring thanthey raise. Despite the apparent energetic waste of such areproductive tactic, overproduction may be favored by naturalselection in some cases. One such case is when surplus offspringcan serve as replacements, or insurance, for failed siblings.We tested the Insurance Egg Hypothesis (IEH) as an explanationfor the overproduction of offspring in an obligately siblicidal seabird, the Nazca booby (Sula grant)i, which fledges a maximumof one nestling regardless of its clutch size. We manipulatedclutch sizes within the range of natural variation encounteredin this species (one-two eggs). The IEH predicts that parentswith two-egg clutches should have higher reproductive successthan those with one-egg clutches because the second egg canprovide a nestling when the first egg fails to hatch, or when the first chick dies young. Consistent with the IEH, naturalone-egg clutches that were enlarged to two eggs produced morehatchlings and fledglings than control one-egg clutches did,and natural two-egg clutches that were reduced to one egg producedfewer hatchlings and fledglings than control two-egg clutchesdid. We also evaluated aspects of the Individual Optimization Hypothesis, which proposes that individual optimal clutch sizesdiffer, as an explanation for clutch size variation in thisspecies. In Nazca boobies, selection driven by replacementvalue appears to favor clutches larger than one even thoughfinal brood size is invariably one. One-egg clutches may be produced by parents experiencing some proximate limitation,such as a lack of food.     

The optimal shape of avian eggs

1. The shape of avian eggs is often explained by involving the mechanical properties of eggshell such as resistance to breakage or invoking physiological forces operating during egg development.
2. Here we take a different approach and investigate the efficient use of space. According to this approach the optimal egg shape is the one that produces the most compact fit under the incubating parent.
3. We extend the model of Andersson (1978) and use a numerical technique to investigate egg shapes in clutches of 1 to 10 eggs. In our model the shape of eggs is described by four parameters in a two-dimensional space. These parameters are free to vary – but eggs cannot be concave.
4. The optimal egg shape for each clutch size was found by a genetic algorithm.
5. The model predicts that egg shape should depend on clutch size. In particular, if the clutch consists of one egg then this egg should be spherical; whereas in clutches of two or three eggs the eggs should be biconical. In clutches of four the eggs should be pointed. The model also predicts that in clutches of over seven eggs the optimal egg shape should be approximately spherical.
6. These predictions are valuable because they point out that some of the variation in avian egg shapes may be explained solely by the efficient use of the brood patch area of the incubating parent.     

Manipulation of laying effort reveals habitat-specific variation in egg production constraints in Great Tits (Parus major)

It has been suggested that a bird's clutch size is not limited by the amount of resources available at the time of laying but that differences in the availability of food for nestlings is the ultimate underlying factor determining spatio-temporal variations in clutch size. However, habitat-related variations in egg production ability has yet to be investigated explicitly. We studied the breeding of Great Tits Parus major in deciduous and coniferous forests in the same area. The sizes of both the clutches and the eggs were, on average, larger in the former habitat than in the latter. A number of females were induced to lay more eggs than usual by removing four eggs from designated experimental clutches early in the laying period. These manipulated females laid approximately one egg more than control females, with the number of additional eggs laid not differing between the habitats. However, in both study years the relative size of the extra eggs – relative to the mean size of earlier laid eggs of the same clutch – was smaller in the coniferous habitat than in the deciduous habitat, while there was no habitat-related difference in the relative size of the last-laid eggs of control clutches. This result indicates that some form of proximate limitation during egg-laying period can contribute to the relatively small clutches and eggs in the coniferous habitat. Our results emphasize the need to take egg production costs into account when attempting to account for spatial variation in the reproductive behaviour of birds.