The relationship between egg size and posthatching development in the thick-billed murre.
Positive relationships between egg size and measures of offspring fitness have been demonstrated in many vertebrates including fish (e.g., Hutchings 1991), amphibians (e.g., Kaplan 1980), and reptiles (e.g., Sinervo 1990). The relationship between egg size and offspring fitness probably has been examined most frequently in birds (reviewed in Williams 1994). Many studies have reported that chicks that hatched from larger eggs experienced higher survival (e.g., Moss et al. 1981, Galbraith 1988, Grant 1991), or faster growth (e.g., Birkhead and Nettleship 1982, Furness 1983), than those from smaller eggs. However, most of the avian studies have been nonexperimental, and their potential shortcomings are well known (Mueller 1990, Williams 1994). Two common criticisms are: (1) that egg size can vary within as well as among clutches, making it difficult to distinguish between these two sources of variation, and (2) that parental quality might have an overriding influence on both egg size and offspring fitness. Experimentation is required to assess whether egg size influences survival or growth independently of parental effects, and studies on species that lay one-egg clutches are likely to be most revealing.
Large eggs have been found to be more likely to hatch than small eggs in some experimental studies (Croxall et al. 1992, Magrath 1992, Amundsen et al. 1996), but not in others (Ollason and Dunnet 1986, Reid and Boersma 1990, Bolton 1991, Amundsen 1995, Smith et al. 1995). Egg size influenced posthatching survival in Lesser Black-backed Gulls, Larus fuscus, but only if the small, last-laid eggs were included in the analysis (Bolton 1991). In contrast, egg size had little effect on survival in the Fulmar, Fulmarus glacialis (Ollason and Dunnet 1986), and Short-tailed Shearwater, Puffinus tenuirostris (Meathrel et al. 1993), two species that lay one-egg clutches. In some studies, egg size determined mass or linear dimensions immediately after hatching, but these initial differences tended to disappear quickly (Amundsen and Stokland 1990, Reid and Boersma 1990, Smith et al. 1995). In other studies, effects of egg size on chick mass or size persisted longer, but there was no effect on growth rate, and the chicks were not measured through to the age of nest departure (Magrath 1992, Amundsen et al. 1996). In his review, Williams (1994) concluded that there was little unequivocal evidence to suggest that large eggs increase offspring fitness in birds.
The Alcidae is a family of marine birds that exhibits unparalleled variation in posthatching developmental strategies (Sealy 1973, Gaston 1985, Ydenberg 1989, Starck and Ricklefs 1998). At one extreme, young pre-cocial alcids (Synthliboramphus spp.) are not fed at the nest and depart to sea at 2 d of age, accompanied by both parents. At the other extreme, young semiprecocial alcids remain at the nest for extended periods and are independent of their parents when they depart to sea at [greater than]50% of adult mass. Two genera (Uria and Alca) employ a strategy that is intermediate between the extremes and unique to the Alcidae: the young remain at the nest for 15-30 d before going to sea at [less than]30% of adult mass, accompanied only by their male parent. As the nestling period of these intermediate alcids is relatively brief, and because egg size effects in other taxa tend to diminish as nestlings age (e.g., Reid and Boersma 1990), egg size might have greater consequences for intermediate alcids than for species that remain longer at the nest.
Thick-billed Murres, Uria lomvia, are intermediate alcids of Arctic waters that nest densely on cliff ledges. They lay a one-egg clutch, and egg size increases with female age to 8 yr (Hipfner et al. 1997), which is typically a mother's 3rd or 4th yr of breeding (Gaston et al. 1994). Younger mothers tend to lay later in the season, so that egg size often declines with laying date (Birkhead and Nettleship 1982, Gaston et al. 1983). However, older females that lay late produce full-sized eggs, suggesting that age or experience, rather than laying date, influences egg size (Hipfner et al. 1997). Birkhead and Nettleship (1982) found that hatching mass (largely predicted by egg size) correlated positively with mass at nest departure in Thick-billed Murres. They proposed that egg size influenced posthatching growth rate in this species, but they also recognized that the relationship might reflect a positive phenotypic correlation between egg size and other parental attributes. For example, a female Thick-billed Murre that forages efficiently (perhaps an older, more experienced bird) might produce a large egg and also feed her chick so well that it grows more rapidly.
In this study, we examine the relationship between egg size and posthatching growth in the Thick-billed Murre. To disengage any possible relationship between egg size and parental attributes, we randomly switched eggs among pairs, and then measured growth in mass and wing length of chicks from hatching until nest departure. For comparison, egg size and growth of control chicks raised by their own parents were measured as well. If there are direct effects of egg size on posthatching growth, then these should be detectable in the experimental chicks. Conversely, if egg size merely reflects parental quality (e.g., foraging skill), then egg size effects should disappear in the experimental chicks. In that case, we would expect positive relationships between the size of eggs laid by the experimental females and the growth of the chicks that hatched from the eggs they fostered.
MATERIALS AND METHODS
The study was conducted in 1994 and 1995 at the Thick-billed Murre colony of 30 000 pairs at Coats Island, Northwest Territories, Canada (62 [degrees] 57 [minutes] N, 82 [feet] 00[minutes] W).
Just prior to the start of hatching, we mapped and numbered the locations of sites occupied by 50 breeding pairs (those that had an egg) on a plot that we could reach relatively easily. Different plots were used in the two years. Every egg was marked with its site number in permanent ink, and the length and maximum breadth was measured to within 0.1 mm using vernier calipers. An egg volume index (length x [breadth.sup.2]) that has a strong linear relationship with fresh egg mass in Thick-billed Murres (r = 0.952, Birkhead and Nettleship 1984) was used as a measure of egg size. The eggs were redistributed randomly among sites on the plot, after being measured, so that for each pair we knew both the size of the egg they had originally laid, and the size of the egg they fostered. All eggs were rechecked before hatching began, to ensure that they were still at the sites where they had been placed during the switch.
These experimental sites were checked between 0900 and 1200 at 2-d intervals (rather than daily, to reduce disturbance) during the hatching and fledging periods, but occasionally at 3-d intervals and once at a 4-d interval during the mid-chick-rearing period (weather conditions sometimes forced a delay). As in previous studies of Thick-billed Murres (e.g., Birkhead and Nettleship 1982), eggs that were known to have been pipped on day (i) and hatched on day (i + 2) were assumed to have hatched on day (i + 1), unless the chick was wet or the down still matted (indicating that it hatched early on day [i + 2]). In the three instances ([approximately]5% of all chicks involved) when we were unsure, chicks with wing lengths [less than]26 mm were assumed to have hatched that day. As wing length at hatching varies little in Thick-billed Murres, with little effect of egg size, these methods should not introduce systematic biases into our estimates of hatching dates nor into the analysis of egg size effects on subsequent wing growth. On one occasion in 1994, when checks had to be delayed to 3 d apart, three chicks that we believed had hatched 2 d previously were found. Consequently, sample sizes for parameters that involve a measurement [TABULAR DATA FOR TABLE 1 OMITTED] of 2-d-old chicks (i.e., growth between 2 and 14 d) are smaller than those for other parameters. Each chick was marked with a binary code of claw clipping, and banded within 1 wk of hatching. On all visits, chicks were weighed to within 1 g with a 300-g spring balance, and the right wing was measured to within 1 mm from the carpus to the tip of the longest feather with the wing held flat and straight along a ruler. We also measured egg size and growth of control chicks raised by their own parents, using the same protocol (Hipfner 1997).
Larger samples were available for 2-d-old than for 1-d-old chicks, because 2-d measurements could be estimated from measurements at 1 and 3 d of age using linear interpolation. Therefore, we used 2-d measurements as estimates of initial size. Only chicks that survived [greater than]14 d were included in the analyses (N = 33 experimental and 57 control chicks in 1994; N = 27 experimental and 56 control chicks in 1995), because 15 d is the youngest age at which Thick-billed Murre chicks are known to depart the nest of their own volition (Gaston and Nettleship 1981). Consequently, 14 d is the oldest age at which a sample is unbiased by the departure of some chicks. Linear interpolation was used to estimate 14-d measurements for chicks not measured at exactly this age.
The following definitions are used: Control Volume is the volume index of the eggs laid by control females; Initial Volume is the volume index of the eggs originally laid by experimental females; Foster Volume is the volume index of the eggs that experimental pairs received after the egg switch; Mass Growth and Wing Growth are the changes in mass and wing length of chicks between 2 and 14 d of age; 14-d Mass and 14-d Wing are masses and wing lengths of chicks at 14 d of age; Departure Mass and Departure Wing are masses and wing lengths of chicks on the last check before departure; Departure Age is the age of the chick at this last check + 1 d. (As in previous studies, we assumed that the chick departed on the day between visits.)
We analyzed measures of chick growth in relation to Control, Initial, and Foster Volume using least squares linear regression; the residuals from all regressions were plotted to ensure approximate normality. We used t tests to compare growth between years, after ensuring that the assumptions of normality and equality of variances were upheld. All probability values are two tailed.
Foster chick masses at 2 d of age were unrelated to Initial Volume ([r.sup.2] [less than] 0.01 in both years), whereas masses at 2 d increased with Foster Volume ([r.sup.2] = 0.32 in 1994 and [r.sup.2] = 0.34 in 1995; ANCOVA, Foster Volume [F.sub.1,53] = 25.93, P [less than] 0.001). Consequently, the egg switches did randomize the relationship between egg size (i.e., Foster Volume) and parent quality (i.e., Initial Volume). Hatching spanned 22 d in 1994 and 12 d in 1995, but hatching date did not influence either Mass Growth ([r.sup.2] = 0.02 in 1994 and [r.sup.2] [less than] 0.01 in 1995; ANCOVA, hatching date [F.sub.1,53] = 0.23, P = 0.63) or Wing Growth ([r.sup.2] = 0.02 in 1994 and [r.sup.2] [less than] 0.01 in 1995; ANCOVA, hatching date [F.sub.1,53] = 0.03, P = 0.87). This suggests that manipulating the timing of breeding (e.g., the duration of incubation) did not systematically influence the experiment.
Interyear variation in growth
Control chicks. - Details and comparisons of egg size and measures of the growth of the control chicks in the two years are provided in Hipfner (1997). Control Volumes were similar in the two years, but Mass Growth, Wing Growth, 14-d Mass, 14-d Wing, Departure Mass, and Departure Wing were higher in 1994 than in 1995. Furthermore, Departure Age was lower in 1994 than in 1995 (Hipfner 1997).
Experimental chicks. - Details and comparisons of egg size and measures of the growth of the experimental chicks in the two years are provided in Table 1. Both Initial and Foster Volumes were similar in 1994 and 1995. Mass Growth and 14-d Mass were higher in 1994, but Departure Mass did not differ between years. Likewise, there were no differences between years in Wing Growth, or 14-d or Departure Wing, and little indication that Departure Age differed between years.
[TABULAR DATA FOR TABLE 2 OMITTED]
Chick growth in relation to Control and Foster Volumes
Control chicks. - Most measures of chick growth tended to increase with Control Volume in 1994 and 1995, with little between-years difference in elevation or slope (Table 2). There was a significant positive relationship between 14-d Mass and Control Volume, and the relationship between Departure Mass and Control Volume approached significance with a test of moderate power (1 - [Beta] = 0.49). However, there appeared to be less effect on Mass Growth. Similarly, despite there being little overt effect of Control Volume on Wing Growth, both 14-d Wing and Departure Wing increased with Control Volume (Table 2).
Experimental chicks. - The slopes of the lines relating Mass Growth, 14-d Mass, and Departure Mass to Foster Volume differed between 1994 and 1995 (Table 3), precluding use of ANCOVA. The slopes of all three relationships were negative in 1994, although none was significant (P = 0.10 to 0.66). In 1995, all three relationships were positive, that between 14-d Mass and Foster Volume being significant ([F.sub.1,25] = 5.11, P = 0.03). Although the relationships between growth in mass and Foster Volume were inconsistent, Wing Growth, 14-d Wing, and Departure Wing all increased strongly with Foster Volume (Table 3, [ILLUSTRATION FOR FIGURE 1 OMITTED]). None of the relationships differed in elevation or slope in the two years, although the differences approached significance [TABULAR DATA FOR TABLE 3 OMITTED] for Departure Wing (Table 3) with tests of moderate power (year: 1 - [Beta] = 0.40; interaction: 1 - [Beta] = 0.42).
To determine how egg size affected wing growth among the experimental chicks, we plotted wing length against chick age between 2 and 14 d for chicks that hatched from the largest one-third of the sample of eggs, and from the smallest one-third of eggs. As the relationships between Wing Growth and Foster Volume differed very little in elevation or slope between 1994 and 1995 (Table 3), we combined data from the two years. The largest one-third of eggs averaged 17% larger than the smallest one-third of eggs (Table 4). Mass Growth of large- and small-egg chicks was similar, but Wing Growth was higher in the large-egg chicks (Table 4). Mean wing lengths differed by 0.5 mm between the two groups at 2 d of age [ILLUSTRATION FOR FIGURE 2 OMITTED], confirming that there is little effect of egg size on hatching wing length (see also Birkhead and Nettleship 1982). The difference in wing length between the two groups increased slowly to 1.5 mm at 6 d of age, when the wings of large-egg chicks began to grow quickly, then increased rapidly to 6.6 mm between 6 and 10 d of age before leveling off by 12 d [ILLUSTRATION FOR FIGURE 2 OMITTED]. Six d is the youngest age at which the primary coverts (the longest feathers of the wing in nestling murres) burst from the sheaths in Thick-billed Murres (Gaston and Nettleship 1981). Fig. 2 indicates that this occurred [approximately]2 d later in small-egg chicks than in large-egg chicks.
Chick growth in relation to Initial Volume
There was very little relationship between any measure of foster chick growth and Initial Volume (Table 5). However, all measures of growth had positive relationships with Initial Volume in 1994, whereas five out of six of the relationships were negative in 1995. The between-years difference in the elevation of the line relating Departure Wing to Initial Volume was significant, and the difference in slope approached significance (Table 5) with a test of moderate power (1 [Beta] = 0.51).
Consequences of variation in chick growth
To investigate whether a chick's growth affects the age at which it leaves the nest, Departure Age was regressed against 14-d Mass and 14-d Wing. Departure Age declined with 14-d Wing in 1994 in both the experimental and control samples (Table 6). In contrast, there was little relationship between Departure Age and 14-d Mass in any experimental or control sample, and little relationship between Departure Age and 14-d Wing in 1995. As hatching date often influences the age at which Thick-billed Murre chicks depart the nest (Hipfner and Gaston 1999), we added this variable into multiple regression models. In these full models, Departure Age still declined significantly with 14-d Wing in 1994 in both the experimental sample ([R.sup.2] = 0.30, [F.sub.2,30] = 6.38, P = 0.005; 14-d Wing P = 0.013, hatching date P = 0.010) [TABULAR DATA FOR TABLE 4 OMITTED] and the control sample ([R.sup.2] = 0.15, [F.sub.2,54] = 4.61, P = 0.014; 14-d Wing P = 0.015, hatching date P = 0.091).
Early development of the wing feathers was enhanced in experimental Thick-billed Murre chicks that hatched from large eggs, compared to those from small eggs. The primary coverts burst from the sheaths [approximately]2 d earlier in large-egg chicks, and the difference in feather lengths created by this effect was maintained at least until the age at which chicks might normally begin to leave the nest. Wing length at 14 d of age and at nest departure also increased with egg size among control chicks, although there was less effect on the rate of wing growth. This positive effect of egg size on wing feather growth has not been observed in other [TABULAR DATA FOR TABLE 5 OMITTED] species of birds (Williams 1994), suggesting that it might reflect adaptations to the intermediate developmental strategy employed by murres, in which rapid development during a brief nestling period is probably critical (Birkhead 1977).
There was little effect of egg size on Mass Growth, the slopes of the lines differing in direction between years, among the experimental chicks. The causes and biological significance of these differences are unclear to us. However, they provide strong evidence that egg size does not influence posthatching growth in mass in Thick-billed Murres, as found in experimental studies on other species (Amundsen and Stokland 1990, Reid and Boersma 1990, Bolton 1991, Magrath 1992, Smith et al. 1995, Amundsen et al. 1996). However, egg size strongly predicted hatching mass, and the 14-d Masses of the fostered chicks also increased with egg size in 1995. Similarly, masses at 14-d and at nest departure both tended to increase with egg size among control chicks, as observed at other Thick-billed Murre colonies (Birkhead and Nettleship 1982). Our data suggest that these mass advantages persisted from hatching mainly as absolute additions, because: (1) egg size had little effect on Mass Growth; and (2) the size of the eggs that the experimental females laid did not predict the growth of the chicks they fostered, i.e., parents that laid large eggs did not necessarily raise fast-growing chicks (the weak relationships between egg size and growth in mass of control chicks agrees with this). Similar persistent effects of egg size on chick mass have been demonstrated in other species of birds (Magrath 1992, Amundsen et al. 1996).
[TABULAR DATA FOR TABLE 6 OMITTED]
The relationship between egg size and feather growth
It has been suggested that the availability of the sulfur amino acids limits rates of egg production in some birds (Murphy 1994, Houston et al. 1995), and also limits rates of feather production during molt (Murphy and King 1992). Lesser Black-backed Gulls provided with supplemental, high-quality protein produced larger third-eggs because the yolk protein content of these eggs was increased (Bolton et al. 1992). Yolk protein is used by the chick to produce its feathers (Romanoff and Romanoff 1949). In murres, variation in egg size is manifested mainly in the mass of the yolk sac that the chick retains at hatching (Birkhead and Nettleship 1984). Consequently, one possible explanation for why Thick-billed Murre chicks that hatched from large eggs had their wing feathers grow quickly is that large-egg chicks hatched with larger yolk sacs that provided them with greater reserves of the sulfur amino acids.
Chick growth in relation to parent quality, as measured by egg size
The experimental females' original egg sizes did not predict the growth of their foster chicks. This result was found in several previous studies (Amundsen 1995, Smith et al. 1995, Amundsen et al. 1996), whereas others found stronger relationships (Amundsen and Stokland 1990, Reid and Boersma 1990, Magrath 1992). As adult age (and/or experience) positively affects both egg size (Hipfner et al. 1997) and chick growth (de Forest and Gaston 1996) in Thick-billed Murres, a discussion of the weakness of this "parent quality" effect is warranted. Some possible explanations include: (1) egg size might reflect female quality but not male quality, and therefore not the quality of the pair. For example, the mates of females that are relatively poor at finding food (and therefore lay small eggs) might compensate by increasing their own provisioning rates. However, Thick-billed Murres tend to mate assortatively with respect to age (Gaston et al. 1994), suggesting that this might be unlikely; (2) egg size varies considerably even among older females (Hipfner et al. 1997). This, combined with the fact that few young birds retain their eggs until late incubation (de Forest and Gaston 1996) when the eggs were switched, might mean that many small-egg pairs were composed of experienced birds. We did not know the ages of adult birds in this study, but based on concurrent observations of undisturbed birds of known age and known egg size, we suggest that this is a strong possibility; and (3) producing a large egg might be taxing to the female, so that a large-egg female might invest less in foraging for her chick, i.e., there may be a trade-off between egg production and chick provisioning (Heaney and Monaghan 1995). That trade-off might be more evident when food is less available, because provisioning the chick becomes more demanding under those conditions (Monaghan et al. 1994). Consequently, we might expect a weaker parental effect in years of poor growth. All relationships between the size of eggs that the experimental females produced and measures of their foster chicks' growth were positive in 1994 (the year of faster growth), whereas five out of six were negative in 1995 (the year of slower growth), observations that are qualitatively consistent with this hypothesis.
Implications for Thick-billed Murres
Nest departure in Thick-billed Murres involves a gliding descent from high on a cliff to the sea. The primary coverts act as the principal planing surface during this descent (Gaston and Nettleship 1981). Many chicks die at nest departure because they fail to unite with their parent at sea, often because they descend too steeply off the cliff and strike ledges below, or land on the beach rather than the sea (Williams 1975, Daan and Tinbergen 1979, Gilchrist and Gaston 1997). Consequently, there might be strong selection for murre chicks to reach a threshold wing-length or optimal wing-loading while at the nest (Birkhead 1977, Hedgren 1981, Hatch 1983). Further, murre chicks that remain at the nest site late in the season may be more likely to be taken by predators prior to departure (Hatchwell 1991, Spear 1993, Gilchrist 1995), and in one study were less likely to be resighted at the colony in future years (Harris et al. 1992). This suggests that early departure is advantageous, and could explain why chicks that had long wings at 14 d tended to depart at younger ages (in one of two years). This pattern occurs frequently in studies of Thick-billed Murres (Hipfner and Gaston 1999). Consequently, the enhanced early wing feather growth that is associated with hatching from a large egg might provide a young murre with an important survival advantage.
The fast wing feather growth that we observed in chicks from large eggs also might reflect fast feather growth in general, and this too could be important. Chicks that grow their body plumage quickly might reach thermal independence sooner, and later be capable of departing the nest at younger ages. At Akpatok Island, Northwest Territories, Canada, in 1993, Thick-billed Murre chicks departed at exceptionally low mass, many still covered in down, and showing retarded growth of contour feathers. Despite this, they had wings of normal departure length (G. Chapdelaine, unpublished data; M. Hipfner, personal observation). This suggests that wing growth, rather than more general plumage development, might be most critical to nestling murres.
Finally, the tendency for Thick-billed Murre chicks that hatch from large eggs to remain heavier than those from small eggs might provide them with a further advantage. Hatch (1983) found that heavier Common Murre, Uria aalge, fledglings survived periods of starvation longer. However, we could not examine the relationship between egg size and nestling survival.
Selection on egg size The results of this study suggest that there are likely to be fitness advantages associated with large eggs in Thick-billed Murres. As there appears to be a genetic component to egg size variation in birds (Boag and van Noordwijk 1987), we expect directional selection in favor of large eggs. However, egg size varies substantially even among older female Thick-billed Murres, and older females laid eggs of similar relative size in 1994 and 1995 (Hipfner et al. 1997).
This apparent paradox has been discussed frequently (e.g., Amundsen et al. 1996). As most previous studies have failed to find seemingly important consequences of egg size variation, it has been argued that these might be relatively slight (Smith et al. 1995), or that egg size might represent the pleiotropic expression of alleles that influence more general metabolic processes (Williams et al. 1993). Alternatively, selection might act only on the environmental and not the genetic component of egg-size variation (Price et al. 1988). In addition, small eggs might be favored in some situations, e.g., if they can be formed more quickly (Birkhead and Nettleship 1982), or if conditions for raising young are favorable so that larger eggs, while more expensive for the female to produce, do not add appreciably to offspring fitness (Williams 1994, Smith et al. 1995).
The annual survival of breeding Coats Island Thick-billed Murres is [approximately]90% (Gaston et al. 1994), so that a reduction in female survival that might offset the advantage of producing a large egg probably would be virtually undetectable (if such a trade-off exists). Moreover, data from only two years clearly are inadequate to fully test any hypothesis relating to interyear variation in feeding conditions. Nonetheless, the results of this study have important implications to studies of the evolution of avian egg size and life histories, because we believe that they demonstrate a novel and important effect of egg size on posthatching development. Future research should examine the consequences of egg size both to adults and their offspring, bearing in mind that the effect of egg size on offspring fitness might most profitably be examined in light of the ecology of the species under consideration.
We thank Josiah Nakoolak for excellent assistance in the field in both years, and Grant Gilchrist for the same in 1995. Thanks also to Lynn Peplinski and the staff of the Science Institute of the Northwest Territories, the Canadian Wildlife Service, and the Polar Continental Shelf Project of Natural Resources Canada, for providing logistical support of our field camp. Funding to conduct this research was provided by the Canadian Wildlife Service, the Natural Sciences and Engineering Research Council of Canada, and the Northern Studies Training Program. Finally, our thanks to John Chardine, Hans Damman, Ben Hatchwell, Douglas Mock. Jaroslav Picman, Colleen Cassady St. Clair, Tony Williams, and an anonymous reviewer for advice and comments that greatly improved the paper.
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|Author:||Hipfner, J. Mark; Gaston, Anthony J.|
|Date:||Jun 1, 1999|
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