Maternal effects in the American coot: consequences for offspring growth and survival

In this study, I focus on intraspecific variation in avian egg size and the consequences of this variation to the resources in eggs, use of these resources by embryos, and effects on hatchlings in a population of American coots (Fulica americana). Eggs range in size from 20 to 36 g, and egg yolk, shell and water contents vary isometrically with egg size indicating that all eggs contain the same proportion of these resources, regardless of egg size. The proportion of the egg mass that is due to albumen solids (proteins and amino acids) increases slightly with increasing egg size. Hatchlings from large eggs contain nearly four times the amount of yolk-sac reserves at hatching as hatchlings from small eggs. Embryos developing in large eggs use a smaller proportion of the yolk available to them than embryos developing in small eggs, which accounts for the extra yolk-sac reserves at hatching. Hatchlings from large eggs have proportionately less lean tissue and more body fat that hatchlings from small eggs. The growth of embryos is well described by a sigmoid growth curve, and most of the increases 20 in embryo mass and decreases in yolk mass occur during the last one third of incubation. Morphometric measures of the legs (tarsus and tibia) increase nearly linearly throughout incubation as well as after hatching. In contrast, the head and wing lengths approach a plateau before hatching. After hatching, the head begins to grow nearly linearly, but wing length does not increase appreciably until 2-3 weeks after hatching, then it lengthens rapidly. The small surface area to volume ratio of large versus small eggs may limit oxygen diffusion and metabolism late in incubation. 1 incubated some eggs in hyperoxic and normoxic conditions to evaluate whether metabolic rates late in incubation were limited bv diffusion of oxygen across the eggshell. Metabolic rates of eggs in hyperoxic conditions were greater than metabolic rates of eggs in normoxic conditions during the last two days prior to convective breathing, suggesting that metabolism is compromised by diffusion of oxygen across the shell late in incubation. Hatchlings from the hyperoxic treatment were heavier than hatchlings from the normoxic treatment, and most of this was due to having more water in their tissues. These patterns of variation in resources and their use by embryos provide a better understanding of the functional significance of egg size to offspring. Introduction Life-history theory predicts that as parents increase investments made to individual offspring those young should benefit by having greater fitness through either increased survival or fecundity (Winkler and Wallin 1987, 21 Steams 1992, Bernardo 1996). In birds, egg and hatchling size are measures of parental investments that are relatively easy to quantify. The influence of egg and hatchling size on subsequent growth and survival of juveniles has been explored in a variety of species with mixed results (reviewed in Williams 1994, Amundsen 1995, Smith et al. 1995, Amundsen et al. 1996, Dawson and Clark 1998, Blomqvist et al. 1997, Hipfner and Gaston 1999, Reed et al. 1999, Styrsky et al. 1999). The contribution that egg size makes to subsequent offspring performance may depend on how resources vary with egg size, the use of these resources during development, and the resulting patterns of energy availability and morphological characters of hatchlings from different sized eggs. There are two general consequences of egg size variation to embryonic development: variation in nutritional contents, and variation in physical dimensions. Nutritional resources in eggs are represented by three major components: 1) yolk, most of which is lipid, is the major source of energy for growth, maintenance and activity costs during development (Romanoff 1960, 1967), 2) albumen is primarily water and proteins (Gilbert 1971), and 3) eggshell provides structure, it is a protective barrier to water loss and pathogen entry, and provides calcium for bone growth (Ar and Rahn 1980, Packard and Packard 1984). The absolute and relative amount of each component can vary with egg mass, and intraspecific patterns have been described for a variety of species. In general, large eggs always have absolutely more yolk, albumen and shell than small eggs. However, the proportional amount of these components can vary considerably. Eggs of species with precocial young are more energy dense than eggs of species 22 with altricial young (Carey et al. 1980, Sotherland and Rahn 1987). In species with precocial young, the amounts of yolk, albumen and shell tend to increase isometrically with increasing egg mass. In contrast, within altricial species, large eggs tend to contain proportionately more albumen (water and proteins) and proportionately less wet and dry yolk than small eggs (Williams 1994, Hill 1995). When considering the relationship between egg size as a measure of parental investment and offspring performance, it is the composition of the egg, rather than just its size that may have the most relevant consequences for offspring characters. Intraspecific variation in the composition of bird eggs and hatchlings has been relatively well studied (egg composition: reviewed in Williams et al. 1982, Williams 1994, Hill 1995; see also Slattery and Alisauskas 1995, St. Clair 1996, Bugden and Evans 1997, Kennamer et al. 1997, Heaney et al. 1998; hatchling composition: Ricklefs 1967, Durui 1975, Ricklefs et al. 1978, Ankney 1980, Birkhead and Nettleship 1984, Ricklefs 1984, Alisauskas 1986, Hepp et al. 1987, Rofstad and Sandvik 1987, Duncan 1988, Duncan and Gaston 1988, Thomas and Peach Brown 1988, Slattery and Alisauskas 1995, Visser and Ricklefs 1995, Finkler et al. 1998, Bech and 0stnes 1999). However, patterns of intraspecific variation in embryo growth and embryo metabolism that connect the initial egg components with final hatchling components are not well resolved in birds. Determining patterns of embryo growth and metabolism requires large sample sizes and repeated measurements on individuals over the course of incubation. Egg metabolic rates can be measured with non-destructive samples. 23 however, measuring embryo growth necessitates termination of development. A reasonable estimate of embryo growth can be obtained by measuring growth of sibling embryos at different stages of development. Full siblings share similar genes and maternal egg environments, both of which may affect embryonic growth and development. The relationship between the surface area of the egg and its volume also varies with egg size. Surface area increases approximately to the 0.67 power of volume, thus, large eggs have a smaller surface area relative to their volume than small eggs (Paganelli et al. 1974). This relationship is particularly important with respect to processes that involve diffusion. In avian eggs, the supply of oxygen occurs only by diffusion of gases across the eggshell (Romanoff and Romanoff 1949, Wangensteen et al. 1970/71). Late in incubation, when oxygen consumption of embryos is at its maximum, oxygen supply across the shell may ultimately limit further increases in metabolism (Metcalfe et al. 1984, Stock and Metcalfe 1984), and this limitation should be greater for large eggs relative to small eggs. This hypothesis can be tested experimentally by increasing the gradient for oxygen diffusion across the shell, which should increase metabolism in a diffusion-limited system. In this study I describe variation in egg, embryo and hatchling characters with respect to variation in egg size of the American coot {Fulica americana), a birds whose young are classified as precocial 3 at hatching (active locomotion and motor activity, downy feathered, and fed by parents, Nice 1962, Starck 1993). I describe initial components of yolk, water, shell and albumen sources present in 24 eggs prior to development. I describe trajectories of embryo growth, the pattern of decrease in yolk sac mass, and variation in residual yolks and chick tissues (lean body mass and body fat) at the end of development. I also describe embryo growth and oxygen consumption during the latter half of incubation, and explore how these may be compromised by confinement within the eggshell. These measurements provide an estimate of variation in the amount of nutrients and energy available for development and how they are used, the limitations on growth and metabolic rates of embryos, and the consequences of these patterns to hatchlings of different sized eggs. Methods I studied a population of American coots breeding in the prairie-parkland region south of Minnedosa, Manitoba, Canada (50° 16' N, 99° 50' W) during the 1997,1998 and 1999 breeding seasons (May through July each year). Egg and chick composition I characterized the relationships between egg components and egg size, and hatchling components and egg and hatchling size. For analysis of egg composition I collected 63 fresh eggs from 42 females. I weighed these eggs to the nearest 0.01 g and measured their greatest width and breadth to the nearest 0.1 mm before separating them into their component parts (yolk, albumen and shell with attached membranes) following the techruque described by Ricklefs (1984). Yolk wet mass and eggshell mass were measured directly whereas albumen wet mass was estimated by subtracting the yolk and shell masses from the fresh egg