Energetics of growth in semi-precocial shorebird chicks in a warm environment: the African black oystercatcher, Haematopus moquini

We studied prefledging growth, energy expenditure and time budgets of African Black Oystercatcher, Haematopus moquini, chicks on Robben Island, Western Cape, South Africa. The aim of the study was to investigate the effect of parental feeding on the growth and energetics of semi-precocial shorebird chicks. Chicks reached mean fledging mass, 463 g, in 40 days. The growth rate coefficient of African Black Oystercatcher chicks was 2% below the predicted value for a shorebird species of their body mass, but it was smaller than that of other precocial and semi-precocial shorebirds to date. Resting metabolic rate (RMR, measured through respirometry), daily metabolisable energy (DME), defined as daily energy expenditure (DEE, measured with doubly labelled water) plus energy deposited into tissue (E(tis)), and total metabolisable energy (TME) of African Black Oystercatcher chicks were similar to those expected for a species of their body size. DEE was not influenced by weather (ambient temperature, operative temperature and wind speed), therefore, variations in DEE may be explained by body mass alone. The relative RMR of the African Black Oystercatcher was greater, their TME was approximately the same, their average daily metabolisable energy (ADME) was less, and they spent less time foraging (short periods of parental feeding) and more time inactive than three precocial species in the Western Cape. Therefore, the semi-precocial mode of development of African Black Oystercatcher chicks reduced energy costs from thermoregulation and activity, and they were able to grow relatively faster than precocial, self-feeding shorebird species in similar climatic conditions. The growth rate coefficient of African Black Oystercatcher chicks was smaller than that of Eurasian Oystercatcher, Haematopus ostralegus, chicks, which may be a consequence of differences in body size and latitudinal effects.     

HOW MAMMALS PRODUCE LARGE-BRAINED OFFSPRING

Two explanations for species differences in neonatal brain size in eutherian mammals relate the size of the brain at birth to maternal metabolic rate. Martin (1981, 1983) argued that maternal basal metabolic rate puts an upper bound on the mother's ability to supply energy to the fetus, thereby limiting neonatal brain size. Hofman (1983) proposed that gestation length in mammals is constrained by maternal metabolic rate, implying an indirect constraint on neonatal brain size. Since individuals of precocial species have much larger neonatal brain sizes and are gestated longer for a given maternal body size than individuals of altricial species, Martin's and Hofman's ideas also require that mothers of precocial offspring have higher metabolic rates for their body sizes than mothers of altricial offspring. Data on 116 mammal species from 13 orders show that neither neonatal brain size nor gestation length is correlated with maternal metabolic rate when maternal body-size effects are removed. For a given maternal size, there is no difference in metabolic rates between precocial and altricial species, despite a two-fold difference between them in average neonatal brain size. However, neonatal brain size is strongly correlated with gestation length and litter size, independently of maternal size and metabolic rate. Analyses conducted within orders replicated the findings for gestation length and suggested that neonatal brain size may be at best only weakly related to metabolic rate. Differences in neonatal brain size appear to have evolved primarily with species differences in gestation length and litter size but not with differences in metabolic rate; large-brained offspring are typically produced from litters of one that have been gestated for a long time relative to maternal size. We conclude that species differences in relative neonatal brain size reflect different life-history tactics rather than constraints imposed by metabolic rate.     

Resting metabolic rate and erythrocyte morphology in early development of thermoregulation in the precocial grey partridge (Perdix perdix)

In the early stages of development of thermoregulation in grey partridge, a typical precocial species, I measured the resting metabolic rate (RMR) and body temperature (Tb) in the thermoneutral zone (TNZ) and the parallel changes in the size of erythrocytes and their cell nuclei. The strong positive correlation between the mass-independent (residuals versus body mass) values of Tb and RMR indicates a close relationship, between these physiological parameters in the first week of life of partridges. In the ontogeny of this species, the dimensions of erythrocytes correlated inversely with the mass-specific metabolic rate (expressed in mW g(-1)), claiming its status as an important and metabolically useful measure of development. The correlation coefficient of these two variables, at the level of individual development within a species, has been further enhanced in the inter-specific analysis at the level of the order Galliformes. The characteristics of changes in the erythrocyte size, in parallel with the dynamics of the resting level of heat production development, in the important period when the thermoregulation is assuming its form in precocial birds, supply new data pertaining to this strategy of avian development.     

Energy metabolism and thermoregulation in hand-reared chukars (Alectoris chukar)

Metabolic rate and colonic temperature were measured in chukars between 1st and 108th day of life (divided into six age groups: 1-3-days old, 1, 2, 3, and 4-weeks old and 3.5-months old) in ambient temperatures set separately for each group and ranging from -12 to 41 degrees C. The Gompertz growth constant for growing chukars (0.042) was close to the value obtained in earlier study for the grey partridge. Similarly as in other species of Galliformes, newly hatched chukar chicks had lower T(b) at TNZ (39.5 degrees C) than that found in older birds (41.3 degrees C in 4-weeks old). The body temperatures taken at TNZ in 2-weeks old chicks and older fitted neatly within allometrically predicted limits of body temperatures for adult birds. The values of RMR at TNZ followed closely a biphasic pattern, with the second phase correlating strongly with the body mass. The value of metabolic scope (the level of metabolic efficiency) for the youngest group was high (3.2) and exceeded the values obtained in earlier studies for other gallinaceous species, including the grey partridge. The obtained values of minimum wet thermal conductance for growing chukar chicks exceeded the predicted values by approximately 40% but the slopes of both lines were very similar. In chukars, the key stage in the expression of fully developed thermoregulatory capacities comes immediately after the first week of life (maintaining somewhat constant body temperature, evident drop in the value of RMR at TNZ and minimal thermal conductance). The model of gradual development of thermoregulation which could be derived from the experiments on chukar chicks was characteristic for typical precocial birds.     

Comparative analyses of the influence of developmental mode on phenotypic diversification rates in shorebirds

Phenotypic diversity is not evenly distributed across lineages. Here, we describe and apply a maximum-likelihood phylogenetic comparative method to test for different rates of phenotypic evolution between groups of the avian order Charadriiformes (shorebirds, gulls and alcids) to test the influence of a binary trait (offspring demand; semi-precocial or precocial) on rates of evolution of parental care, mating systems and secondary sexual traits. In semi-precocial species, chicks are reliant on the parents for feeding, but in precocial species the chicks feed themselves. Thus, where the parents are emancipated from feeding the young, we predict that there is an increased potential for brood desertion, and consequently for the divergence of mating systems. In addition, secondary sexual traits are predicted to evolve faster in groups with less demanding young. We found that precocial development not only allows rapid divergence of parental care and mating behaviours, but also promotes the rapid diversification of secondary sexual characters, most notably sexual size dimorphism (SSD) in body mass. Thus, less demanding offspring appear to facilitate rapid evolution of breeding systems and some sexually selected traits.     

Altricial and precocial developmental features in modern meat-type chicks

Variability of egg weight, egg yolk content, neonatal growth rate and relationships of these parameters were studied in meat-type chicks. As it had been established the level of variability in neonatal growth traits was greater than variability of the egg morphology parameters. Egg weight had stronger influence on the chicks' neonatal growth rate than egg yolk content did. Low egg size was associated with limited neonatal growth rate variability, declined chick weight at hatching and increased relative growth rate throughout four days post hatch. Comparison of egg morphological parameters in two species having the same female definitive body weight--meat-type domestic fowl (precocial type) and brown pelican (altricial type) has shown, that, in contrary to predicted on the basis of avian developmental typology, egg weight to female body ratio was greater in brown pelican, egg yolk content was equal in both species.     

Catabolic capacity of the muscles of shorebird chicks: maturation of function in relation to body size

Newly hatched precocial chicks of arctic shorebirds are able to walk and regulate their body temperatures to a limited extent. Yet, they must also grow rapidly to achieve independence before the end of the short arctic growing season. A rapid growth rate may conflict with development of mature function, and because of the allometric scaling of thermal relationships, this trade-off might be resolved differently in large and small species. We assessed growth (mass) and functional maturity (catabolic enzyme activity) in leg and pectoral muscles of chicks aged 1-16 d and adults of two scolopacid shorebirds, the smaller dunlin (Calidris alpina: neonate mass 8 g, adult mass 50 g) and larger whimbrel (Numenius phaeopus; neonate mass 34 g, adult mass 380 g). Enzyme activity indicates maximum catabolic capacity, which is one aspect of the development of functional maturity of muscle. The growth rate-maturity hypothesis predicts that the development of catabolic capacity should be delayed in faster-growing muscle masses. Leg muscles of both species were a larger proportion of adult size at hatching and grew faster than pectoral muscles. Pectoral muscles grew more rapidly in the dunlin than in the whimbrel, whereas leg muscles grew more rapidly in the whimbrel. In both species and in both leg and pectoral muscles, enzyme activities generally increased with age, suggesting increasing functional maturity. Levels of citrate synthase activity were similar to those reported for other species, but l-3-hydroxyacyl-CoA-dehydrogenase and pyruvate kinase (PK) activities were comparatively high. Catabolic capacities of leg muscles were initially high compared to those of pectoral muscles, but with the exception of glycolytic (PK) capacities, these subsequently increased only modestly or even decreased as chicks grew. The earlier functional maturity of the more rapidly growing leg muscles, as well as the generally higher functional maturity in muscles of the more rapidly growing dunlin chicks, contradicts the growth rate-maturity function trade-off and suggests that birds have considerable latitude to modify this relationship. Whimbrel chicks, apparently, can rely on allometric scaling of power requirements for locomotion and the thermal inertia of their larger mass to reduce demands on their muscles, whereas dunlin chicks require muscles with higher metabolic capacity from an earlier age. Thus, larger and smaller species may adopt different strategies of growth and tissue maturation.     

Effects of weather on the survival and growth of Corncrake Crex crex chicks

Weather conditions during the early life of precocial chicks of some bird species have marked effects on survival and may also cause changes in adult population size. In this paper, we use data from broods with radiotagged mothers to examine correlations of growth rates and survival of Corncrake Crex crex chicks in Scotland and Ireland with temperature and rainfall. The loss of whole broods before they reached independence was infrequent and not correlated with temperature or rainfall. Loss of some chicks from broods before independence usually occurred and multiple regression analysis indicated that the proportion of chicks that survived increased with decreasing initial brood size, increasing temperature and decreasing rainfall. However, the magnitude of the effects of weather on survival were quite small. The rate of weight gain of chicks varied considerably within and among broods. The mean daily weight gain rate of broods decreased significantly with increasing rainfall, and variation in the weight of chicks within broods was greater for broods whose mean rate of weight gain was low.     

Relationship of hepatocyte ploidy levels with body size and growth rate in mammals.

To elucidate possible causes of the elevation of genome number in somatic cells, hepatocyte ploidy levels were measured cytofluorimetrically and related to the organismal parameters (body size, postnatal growth rate, and postnatal development type) in 53 mammalian species. Metabolic scope (ratio of maximal metabolic rate to basal metabolic rate) was also included in 23 species. Body masses ranged 10(5) times, and growth rate more than 30 times. Postnatal growth rate was found to have the strongest effect on the hepatocyte ploidy. At a fixed body mass the growth rate closely correlates (partial correlation analysis) with the cell ploidy level (r = 0.85, P < 10(-6)), whereas at a fixed growth rate body mass correlates poorly with ploidy level (r = -0.38, P < 0.01). The mature young (precocial mammals) of the species have, on average, a higher cell ploidy level than the immature-born (altricial) animals. However, the relationship between precocity of young and cell ploidy levels disappears when the influences of growth rate and body mass are removed. Interspecies variability of the hepatocyte ploidy levels may be explained by different levels of competition between the processes of proliferation and differentiation in cells. In turn, the animal differences in the levels of this competition are due to differences in growth rate. A high negative correlation between the hepatocyte ploidy level and the metabolic scope indicates a low safety margin of organs with a high number of polyploid cells. This fact allows us to challenge a common opinion that increasing ploidy enhances the functional capability of cells or is necessary for cell differentiation. Somatic polyploidy can be considered a "cheap" solution of growth problems that appear when an organ is working at the limit of its capabilities.     

The energetic implications of precocial development for three shorebird species breeding in a warm environment

We investigated the effect of body size, parental behaviour and timing of breeding on the chick growth and energetics of three precocial shorebird (Charadrii) species in a warm sub-tropical environment: the Kittlitz's Plover Charadrius pecuarius , Blacksmith Lapwing Vanellus armatus , and Crowned Lapwing V. coronatus . The three species exhibited slower growth, longer pre-fledging periods and lower energy expenditure during the pre-fledging period than Arctic and temperate zone relatives of similar size. It was found that relative growth rates of charadriid and scolopacid species increased by 1.77% per degree latitude. Blacksmith and Crowned Lapwings are of similar size (i.e. about 160 g), about four times the mass of Kittlitz's Plovers. Taking body mass into account, the resting metabolic rate and daily energy expenditure of the three study species were similar. The relative amounts of energy needed for chicks to grow from a hatchling to a fledgling were low for the three species studied. The relative amount of energy needed to complete growth in charadriid and scolopacid species increased by 2.54% per degree latitude. Because Crowned Lapwings exhibited faster growth than Blacksmith Lapwings but similar daily energy expenditure we suggest that Blacksmith Lapwings compensate for greater energy expenditure in colder weather by growing more slowly. We suggest that small growth rate coefficient, low resting metabolic rate and low daily energy expenditure are adaptations to lower food availability and milder ambient temperatures in sub-tropical breeding habitats compared to temperate or Arctic regions.     

ADAPTATION, CONSTRAINT, AND COMPROMISE IN AVIAN POSTNATAL DEVELOPMENT

1. This paper discusses factors that influence the evolution of growth rate and determine its variation among species of birds. Growth rate is related to evolutionary fitness through the use of time, energy, and nutrients. In addition, balances between factors favouring rapid growth and those favouring slow growth may be investigated directly by experiment and by comparative observation. 2. David Lack (1968) proposed that the growth rate of the young is the optimum balance between selection for rapid growth to reduce the vulnerable period of development and selection for slow growth to reduce the energy requirements of the young. 3. To test Lack's hypothesis, the growth rates of birds, estimated by fitting sigmoid equations to curves relating weight to age, were surveyed widely from the literature. Among all species examined, growth rate was inversely related to adult weight. Among birds of similar size, most variation in growth rate was related to the degree of maturity of the neonate. Altricial chicks, which depend upon their parents for food and warmth, grow more rapidly than precocial chicks, which are self-sufficient shortly after hatching. Lack's hypothesis, which predicts a direct relationship between growth rate and mortality rate, was not supported. 4. I propose that the key to understanding variation in growth rate among birds lies in the balance between rate of cell proliferation or cell growth, on one hand, and acquisition of mature function, on the other. This idea is consistent with principles of cellular and developmental biology. It is supported by comparisons of (a) the neonates of different species, (b) the individual over the course of the developmental period, and (c) tissues whose use is acquired at different stages of development, wherein more mature individuals or tissues grow more slowly than those with less developed function. 5. Species of birds that are classified as semi-precocial develop precocially but grow rapidly. Although these seemingly violate the general rule relating growth rate to precocity, a closer inspection of their development reveals that they too support the rule. In the Common Tern, the legs, which are the key organ in precocial development, grow at the expected slow rate. The body as a whole grows rapidly because the growth increment of the legs is small and their growth is completed quickly. 6. Growth rates of precocial birds do not decrease abruptly at hatching. This points more to gradual tissue differentiation than to the pattern of procurement and allocation of energy as the primary control for growth rate. 7. Precocious development is favoured when the chicks are capable of self-feeding or when food supplies are distant from the next site and travelling time between one and the other is long. Precocity of the neonates frees both parents to feed at a distant food source. 8. Some species having diets with low levels of protein or other nutrients may grow slowly in order to match nutrient requirements to their availability in the diet. This pattern is indicated especially among the Procellariiformes, which feed an oily diet to their young, and also among tropical fruit-eating birds. 9. Some tropical, pelagically-feeding sea-birds that rear only one offspring at a time may not be able to procure food sufficient to support rapid chick growth. Alternative explanations for slow growth among these species include difficulty in obtaining essential nutrients and more precocious development of activity than in related species having more rapid growth.     

Ontogenetic development of the ophthalmic rete in relation to brain cooling in chickens and pigeons

The brain cooling capacity of the altricial pigeon increases during posthatching growth at a higher rate than that of the precocial duck and chicken. To determine if this difference between the altricial and the precocial modes of development can be related to growth rates of the vascular heat exchanger involved in brain cooling (the ophthalmic rete), we performed a morphometric analysis of this structure during the post-hatching maturation of the three species. The number of vascular units in the rete did not change during development but differed significantly among species. The retia continued to grow in length and diameter in an exponential relation with body mass at similar rates in all species. The surface area of the retial arteries, which reflects the area available for countercurrent heat exchange, also increased exponentially with body mass, but without significant differences among the three species. However, the effectiveness of the rete in brain cooling, as indicated by the degree of brain cooling per unit of heat-exchange area in the rete, was higher in the altricial pigeon than in the precocial chicken and duck. It is concluded that the posthatching morphometric changes in the ophthalmic rete (rete ophthalmicum) are important for the development of brain cooling capacity, but cannot solely explain differences in brain cooling between growing altricial and precocial birds. These differences are most likely related to differences in the maturation of the central thermoregulatory control system and the peripheral effector mechanisms among the two groups of birds.     

Load Lightening in Southern Lapwings: Group‐Living Mothers Lay Smaller Eggs than Pair‐Living Mothers

Females of some cooperative‐breeding species can decrease their egg investment without costs for their offspring because helpers‐at‐the‐nest compensate for this reduction either by feeding more or by better protecting offspring from predation. We used the southern lapwing (Vanellus chilensis) to evaluate the effects of the presence of helpers on maternal investment. Southern lapwings are cooperative (some breeding pairs are aided by helpers), chick development is precocial, thus adults do not feed the chicks, and adults offer protection from predators through mobbing behaviors. We tested whether southern lapwing females reduced their reproductive investment (i.e. load‐lightening [LL] hypothesis) or increased their investment (i.e. differential allocation hypothesis) when breeding in groups when compared with females that bred in pairs. We found that increased group size was associated with lower egg volume. A significant negative association between the combined egg nutritional investment (yolk, protein, and lipid mass) and group size was observed. Chicks that hatched from eggs laid in nests of groups were also smaller than chicks hatched in nests of pairs. However, there was no relationship between the body mass index of chicks, or clutch size and group size, which suggests that such eggs are, simply, proportionally smaller. Our results support the LL hypothesis even in a situation where adults do not feed the chicks, allowing females to reduce investment in eggs without incurring a cost to their offspring.     

Brood rearing costs affect future reproduction in the precocial common goldeneye Bucephala clangula

Life-history theory assumes a trade-off between current reproductive effort and future reproductive success. There are a large number of studies demonstrating reproductive trade-offs in different animal taxa, particularly in birds. Most bird studies have focused on the costs of chick rearing in altricial species. These costs have been assumed to be low in precocial species, but this aspect has been little studied. We used long-term individual reproductive data from the common goldeneye Bucephala clangula , an iteroparous precocial duck with uniparental female care, to examine whether brood rearing carries costs that affect future reproductive performance. All females were experienced breeders, and possible differences in female quality were ruled out. We compared within-individual (between-year) changes in clutch size, hatching date and body mass between females that had reared a brood in the previous year and females that had not. It turned out that brood rearing involved a cost in terms of clutch size and hatching date the next year, but not in terms of body mass: females that had reared a brood in the previous year laid relatively smaller clutches and laid relatively later than females that had not reared a brood. Our results show that normal brood rearing in a precocial species involves costs that affect future reproduction.     

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

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

Comparative embryonic development of the skeleton of the domestic turkey (Meleagris gallopavo) and other galliform birds

Ossification sequences are poorly known for birds in general, even for common domestic and experimental species. Such sequences constitute a rich source of data on character evolution, and may even provide phylogenetic information. It is not clear, however, what factors influence ossification sequences and what the relative importance of phylogeny is to the sequences. Galliformes constitute a good group to examine these variables. These birds are osteologically conservative, have precocial young, but have a broad spectrum of body sizes and incubation periods. Here, I describe the embryonic ossification of the skeleton in the domestic turkey (Meleagris gallopavo), and compare it to the domestic chicken (Gallus gallus) and the Japanese quail (Coturnix coturnix). Ossification sequences in this group are not affected by egg size or incubation period. They also appear to be independent of both the spatial location and the embryonic tissue from which the osteogenic cells originated. Accumulation of a wider sample of ossification sequences from more morphologically variable avian taxa will be necessary in order to test functional and phylogenetic effects.     

The American Avocet (Recurvirostra americana) as a paradigm for adult automimicry

Summary The body of theory concerning life-history strategies predicts that the duration of high-mortality stages should be minimized by natural selection. This is especially applicable to the avian pre-flight stage, during which growth rates typically are rapid. Using the American Avocet (Recurvirostra americana) as a paradigm, I propose a developmental strategy by which young animals can lower their mortality rates by an accelerated (and deceptive) acquisition of adult or adult-like characters. The benefit accrues when predators misidentify the vulnerable young as adults and fail to attack them because adults are much less vulnerable. This strategy, termed adult automimicry, is most likely to occur in precocial species living in open habitats.American Avocets are large, precocial, open-country shorebirds that first fly when about 4–5 weeks old. They develop a juvenal, plumage in their third week that resembles adult breeding plumage in pattern and color, even though plumage details are different. At this time chicks begin using adult foraging techniques and tend to move away rather than hide from potential predators. A few weeks later they acquire a first winter plumage that resembles adult winter plumage. Thus, avocet chicks appear unusually adult-like after their second week. This should make it difficult for distant predators to distinguish flightless chicks from volant adults.     

Cardiomyocyte ploidy levels in birds with different growth rates

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

Chick growth rates in Charadriiformes: comparative analyses of breeding climate, development mode and parental care

The rate at which a young bird grows is highly diverse across taxa. We investigated the influences of ecological variables on growth rates of shorebirds, gulls and their allies (order Charadriiformes) using comparative analyses of 68 species. We investigated three hypotheses: (1) exposure to cold temperatures results in reduced growth rate due to the increased energy expenditure required for thermoregulation, (2) fast growth rates allow offspring to complete development in habitats with short periods of fair ecological conditions, and (3) parental feeding allows the offspring to grow faster than self-feeding offspring. Charadriiform species are suitable for testing these hypotheses, because they breed in diverse environmental conditions that include Arctic and Antarctic habitats, temperate zones and tropics, and in some species the offspring feed themselves (precocial) whereas in others they are fed by the parents (semi-precocial). First, we tested the influence of ambient temperature on growth rate and we found that species breeding in cold habitats had faster growth rates than species breeding in warm temperatures. The relationship between growth rate and ambient temperature was not significantly different between precocial and semi-precocial offspring. Second, we tested the influence of the length of the breeding season on growth rate, and we found that species with shorter breeding seasons had faster growth rates than species with longer breeding seasons. Finally, we show that precocial offspring grew slower than semi-precocial offspring, and this relationship remains significant when the influences of ambient temperature and breeding season length are statistically controlled. In conclusion, our work, using phylogenetically corrected models, confirms that ambient environment and developmental mode of young together influence the growth of Charadriiform chicks, and their effects are additive.     

Mechanisms promoting higher growth rate in arctic than in temperate shorebirds

We compared prefledging growth, energy expenditure, and time budgets in the arctic-breeding red knot (Calidris canutus) to those in temperate shorebirds, to investigate how arctic chicks achieve a high growth rate despite energetic difficulties associated with precocial development in a cold climate. Growth rate of knot chicks was very high compared to other, mainly temperate, shorebirds of their size, but strongly correlated with weather-induced and seasonal variation in availability of invertebrate prey. Red knot chicks sought less parental brooding and foraged more at the same mass and temperature than chicks of three temperate shorebird species studied in The Netherlands. Fast growth and high muscular activity in the cold tundra environment led to high energy expenditure, as measured using doubly labelled water: total metabolised energy over the 18-day prefledging period was 89% above an allometric prediction, and among the highest values reported for birds. A comparative simulation model based on our observations and data for temperate shorebird chicks showed that several factors combine to enable red knots to meet these high energy requirements: (1) the greater cold-hardiness of red knot chicks increases time available for foraging; (2) their fast growth further shortens the period in which chicks depend on brooding; and (3) the 24-h daylight increases potential foraging time, though knots apparently did not make full use of this. These mechanisms buffer the loss of foraging time due to increased need for brooding at arctic temperatures, but not enough to satisfy the high energy requirements without invoking (4) a higher foraging intake rate as an explanation. Since surface-active arthropods were not more abundant in our arctic study site than in a temperate grassland, this may be due to easier detection or capture of prey in the tundra. The model also suggested that the cold-hardiness of red knot chicks is critical in allowing them sufficient feeding time during the first week of life. Chicks hatched just after the peak of prey abundance in mid-July, but their food requirements were maximal at older ages, when arthropods were already declining. Snow cover early in the season prevented a better temporal match between chick energy requirements and food availability, and this may enforce selection for rapid growth.