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Egg sizes of birds vary considerably at the population
level; the largest eggs are generally at least 50% larger
than the smallest eggs within a population (Christians
2002). Such variation could result from consistent
differences in egg size among individuals. These consis-
tent differences among individuals, in turn, could be
the result of consistent differences in environmental
context (e.g. habitat quality before egg laying) or the
result of genetic and ontogenetic factors that help
determine egg size and differ among individuals (e.g.
female size). On the other hand, it is also possible that
the observed variation in egg size is the result of differ-
ences within individuals, in response to annual varia-
tion in exogenous conditions (e.g. food, precipitation or
Mo A. Verhoeven1,*, A.H. Jelle Loonstra1, Alice D. McBride1, Joost M. Tinbergen1,
Rosemarie Kentie1,2, Jos C.E.W. Hooijmeijer1, Christiaan Both1,
Nathan R. Senner1,3 & Theunis Piersma1,4
Verhoeven M.A., Loonstra A.H.J., McBride A.D., Tinbergen J.M., Kentie R.,
Hooijmeijer J.C.E.W., Both C., Senner N.R. & Piersma T. 2019. Variation in egg
size of Black-tailed Godwits. Ardea 107: 291–302. doi:10.5253/arde.v107i3.a7
As is the case for most avian species, there is considerable variation in the egg
size of Continental Black-tailed Godwits Limosa l. limosa breeding in The
Netherlands. It is interesting that egg size has costs and benefits yet varies
considerably at the population level. To better understand this variation in egg
size, we tested its relationship to a suite of individual and environmental factors.
We found that egg size can decrease up to 2.8% throughout a breeding season
and that egg size increases with clutch size by 1.4% with each additional egg in
the clutch. Female body mass and body size explained 5% of the total variation
in egg size observed across the population. Furthermore, females wintering
south of the Sahara laid 3% smaller eggs than those wintering north of the
Sahara. We also found that egg size increases with age, which may indicate
age-related differences in the endogenous and/or exogenous conditions of
females. The variation in egg size was, however, mostly the result of consistent
differences among individuals across years (repeatability = 0.60). A comparison
of daughters with mothers suggested that most of this individual repeatability
reflects heritable variation (heritability = 0.64). The actual individual traits that
underlie this heritable variation among individuals remain mostly undetermined.
Smaller eggs did have a slightly lower chance of hatching, but we found no rela-
tionship between egg size and chick survival. Finally, nest and chick survival
were strongly correlated with lay date. Thus, in Black-tailed Godwits, lay date
may actually reflect a female’s endogenous and/or exogenous condition at the
moment of egg-laying. This finding may be general across birds, since food
supplementation experiments usually result in advanced laying and larger clutch
sizes rather than in larger eggs.
Key words: age, environmental conditions, body condition, state, parental effort
1Conservation Ecology Group, Groningen Institute for Evolutionary Life
Sciences, University of Groningen, P.O. Box 11103, 9700 CC Groningen, The
Netherlands;
2Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK;
3Department of Biological Sciences, University of South Carolina, 715 Sumter
St., Columbia SC, 29028;
4NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal
Systems and Utrecht University, P.O. Box 59, 1790 AB Den Burg, Texel, The
Netherlands;
*corresponding author (m.a.verhoeven@rug.nl)
Variation in egg size of Black-tailed Godwits
temperature) or changes in endogenous condition (e.g.
female age or body condition). To understand the
causes of variation in egg size, it is therefore necessary
to first partition the variation in egg size into among-
and within-individual differences.
Among- and within-individual differences are
usually partitioned by calculating the repeatability of
egg size (Christians 2002). In previous studies, the egg
size of individual birds has been found to be signi -
ficantly repeatable (mean repeatability = 0.68; 23
studies of 18 species reviewed by Christians 2002). In
other words, in most species, individuals consistently
differ from one another in egg size and show only rela-
tively minor within-individual variation in egg size.
However, in his review, Christians (2002) also con -
cluded that only 10–20% of the variation in egg size
was explained by environmental and among-individual
factors such as food availability, temperature, body size,
age and mass.
Pick et al. (2016a) discovered that Japanese Quails
Coturnix japonica laying larger eggs invested more
energy into their reproductive organs and also had a
higher resting metabolic rate. Larger eggs also gener-
ally contain higher absolute levels of egg components
and produce larger and heavier chicks that survive
better (reviewed in Krist 2011 and Williams 2012).
These results suggest that egg size has costs and bene-
fits, and that individuals might balance these costs and
benefits when allocating resources to egg size. Inte -
r
estingly, since there is large between-individual varia-
tion in egg size and only minor within-individual varia-
tion, the outcome of this potential trade-off must differ
both considerably and consistently among individuals.
That the factors determining this variation among indi-
viduals remain largely undiscovered makes it all the
more intriguing (Christians 2002, Williams 2012). To
further examine the considerable variation in the egg
sizes of birds, we explore the determinants of egg size in
Continental Black-tailed Godwits (hereafter Godwits).
The egg size of Godwits may be particularly inter-
esting to study because this species differs in two ways
compared with most of the 18 species reviewed by
Christians (2002). First, Godwits have a relatively
invariant clutch size of four eggs (87% of all clutches,
n= 6396), and second, the chicks forage for them-
selves (Schroeder et al. 2009, 2012). Thus, most God -
wits do not vary their total parental effort by varying
their clutch size and might instead vary their egg size
more than would species with a variable clutch size.
Furthermore, since they have chicks that forage for
themselves, Godwits are relieved of the energetically
demanding task of food provisioning (but not of
supplemental heating; see Schekkerman et al. 2003).
This means that in terms of allocating parental effort to
reproduction, the effort put into eggs plays a propor-
tionally greater role in Godwits than it does in altricial
bird species (Williams 1994, Starck & Ricklefs 1998). It
is worth noting that the effects of egg size on offspring
phenotype have been found to differ between altricial
and precocial species; in the altricial Blue Tit Cyanistes
caeruleus the effects of egg size dissipate early in
ontogeny (Hadfield et al. 2013), whereas in the preco-
cial Japanese Quail they remain until adulthood (Pick
et al. 2016b).
We are curious about what the variation in egg size
of Godwits reflects and how this might differ from
other bird species. Therefore, we investigated whether
Godwits show variable egg size and related their egg
size to a suite of environmental and individual factors.
First, we estimated the repeatability and heritability of
egg size. Second, we searched for annual and seasonal
patterns in egg size, and then turned to individual
factors such as female size, mass, age, lay date, and
wintering location to explain the variation. Finally to
understand why variation in egg size persists in
Godwits, we explored how egg size and lay date are
associated with nest and chick survival. Our goal is to
better understand the variation in egg size for Godwits
and birds in general.
METHODS
We studied Godwits in southwestern Friesland, The
Netherlands, from 2004 until 2017. In 2004, our study
area was a single 250 ha polder (52°59'55"N, 5°24'31"E).
Polders are historical and hydrological entities charac-
terized by fields with similar water levels (Groen et al.
2012). In 2007, the study area was expanded to 8970
ha in order to include multiple polders; in 2012 the
study area was expanded again to 11,415 ha (see
Groen et al. 2012 and Senner et al. 2015 for a detailed
description of the study area). Each year, we searched
the study area for nests and measured the width and
length of the eggs when a nest was found. We found
most nests during the incubation phase and therefore
measured their egg flotation angles to estimate the lay
date of each nest (van Paassen et al. 1984). For God -
wits, more than 80% of all estimates are accurate
within two days and 95% of all estimates are accurate
within three days (van Paassen et al. 1984). In most
cases we floated two eggs and used the average to
better estimate lay date, but even with this approach
some measurement error persists. To put this measure-
ARDEA 107(3), 2019
292
Verhoeven et al.: VARIATION IN EGG SIZE OF BLACK-TAILED GODWITS
ment error into context, lay dates vary from 32–55 days
within a breeding season. Following Schroeder et al.
(2009), we calculated egg volume using the formula
(length ×width2×0.52); we refer to this as egg size.
In our analyses we use clutch size as a fixed effect, but
we cannot distinguish between partial predation and a
clutch that naturally contained fewer than four eggs. To
ensure that we did not include any clutches that were
still in the laying phase, we included clutches of fewer
than four eggs only when upon initial discovery the
clutch had already been incubated for two or more
days, or when two or more days after its initial
discovery in the laying phase the clutch was being incu-
bated and contained the same number of eggs (thus
excluding any noticeable predation that might have
occurred in the meantime). In this way we excluded
351 clutches that failed before reaching what might
have been their final clutch size. However, our sample
still unavoidably includes clutches that were partially
depredated.
On a subset of the found nests, we caught incuba -
ting adults to individually mark them with colour rings
and take blood for molecular sexing (e.g. Schroeder
et al. 2009). From 2008 onwards, we colour-ringed
recently hatched juveniles as well as juvenile Godwits
that we captured in the study area after they had
already left the nest. For the latter group of juveniles,
we know the year in which they were born but often
not their maternal nest. Our analyses that include juve-
niles or birds with known age are based on data from
2008 onwards. In the years after capture, we tried to
link individual adults to specific nests through visual
observation or, coincidentally, by recapturing them.
However, either because we failed to link the marked
female or because the female was unmarked, our
dataset includes many clutches with unknown females.
It is important to realize that this group of unknown
females also includes marked females that were
successfully linked to nests in other years. To avoid
pseudoreplication we have therefore used in our
analyses only those nests to which a marked female
was linked, meaning that we excluded 4596 clutches
for which the female was unknown in that year. The
sample size of clutches we could include in our
analyses was limited not only by not knowing the iden-
tity of the female, but also by not knowing traits
specific to that female (such as body mass, age and
wintering location). This means that the numbers of
293
Nest of Godwit on fallow field (photo Jan van de Kam, Venray, May 1993).
covariates and clutches vary considerably among
analyses and that we were hardly ever able to estimate
multiple parameters in the same model. To keep track
of what is included in each analysis, we have numbered
every analysis and corresponding result and included
Tables 1 and 2 for a complete overview.
Analysis
All mixed models in this paper use the package ‘lme4’
(Bates et al. 2015) in the R programming environment
(R Core Team 2018). We obtained chi-squared values
for the significance of the fixed effects from likelihood
ratio tests of nested models with and without the vari-
able of interest. We used the function ‘rpt’ which is part
of the R package ‘rptR’ (Stoffel et al. 2017) to estimate
the proportion of variance explained by the fixed
effects of these models and assessed the uncertainty of
these estimates with 1000 parametric bootstraps. We
used a range of models for the analyses of egg size,
which are described next.
(1) Global Model: In this linear mixed effect model
(LMM) we related an individual’s egg size to its lay
date (continuous covariate), clutch size (continuous
covariate) and nesting attempt (three-level factor). The
random intercepts were clutch, individual, year and
polder. In 96% of the cases we were unaware of
whether a nest was a first or second attempt and we
therefore added ‘unknown’ as a third factor level. We
used this model and the function ‘rpt’ to estimate the
adjusted repeatabilities of the different groups specified
as random effects, and assessed the uncertainty of
these estimates with 1000 parametric bootstraps
(Nakagawa & Schielzeth 2010).
(2) Condition Model: In this LMM we related an
individual’s egg size to its lay date, clutch size, body
mass and structural size (all continuous covariates).
The random intercepts were clutch, individual, year
and polder. Body mass was measured during incuba-
tion of the clutch. For ease of comparison to the other
models, we scaled the body mass of individuals by
subtracting the mean and dividing by the standard
deviation. The first principal component was derived
from five linear dimensions: bill length (exposed
culmen; ±0.1 mm), total-head length (±0.1 mm),
wing length (flattened and straightened; ±1 mm),
tarsus length (±0.1 mm) and tarsus-toe length (tarsus
plus mid-toe without claw; ±1 mm), and explained
55% of the variation. We multiplied the first principal
component value by –1 such that it was positively
related to the linear dimensions (i.e. a higher value = a
larger female) and used it as a measure of overall struc-
tural size.
(3) Age Model: In this LMM we related an indi-
vidual’s egg size to its lay date, clutch size, body mass,
structural size and age (all continuous covariates). We
checked whether the model improved when a quadratic
term was added to age, but it did not (+4.3 AICc). The
random intercepts were clutch, individual, year and
polder. For this analysis we could only use individuals
that were ringed as chicks (i.e. of known age) and
recaptured as adults (i.e. of known size and mass). This
limited our sample size to 53 clutches of 40 females. In
order to include an additional 81 clutches of 40 females
for which the age but not the size was known, we also
performed this analysis without body mass and struc-
tural size included as covariates (Age Model 3B). We
did add a quadratic term to age in this analysis because
it improved the model (–11.3 AICc). Although this
model uses a larger dataset, the results could be
misleading because the effects of body condition and
age cannot be disentangled.
(4) Daughter-mother relation: We could correlate
the average egg volume of 49 daughters to that of their
mother. Because egg volume increases with age (see
Results and Discussion), we plotted the relationship
between the egg volumes of daughters and their
mothers for every age of the daughters (Figure 3A).
This suggested that the relationship between daughters
and mothers might only become apparent when the
daughters are three years old or older. To test for this
possibility, we included an interaction with age as a
two-level factor (
≤
2 years old and
≥
3 years old) in a
linear model in which we related the average volume of
daughters to the average volume of their mothers
(continuous covariate). This interaction was not signifi-
cant (see Results) and we therefore averaged the egg
size of daughters across all their ages and related this to
the average egg size of their mother in a linear model.
We estimated the heritability of egg size as two times
the slope of this linear regression (Becker 1984). Such
parent-offspring regressions with small sample sizes
(n< 100 pairs) are imprecise and may overestimate
heritability (de Villemereuil et al. 2013). However, we
lack the sample size and pedigree information needed
for a more precise analysis.
(5) Wintering Model: In this LMM we related an
individual’s egg size to its lay date, clutch size, body
mass, structural size (continuous covariates) and
wintering location (two-level factor). The random
intercepts were clutch, individual, year and polder.
Individual Godwits consistently winter either north or
south of the Sahara (Verhoeven et al. 2019). To deter-
mine whether this consistent migratory behaviour
results in consistent differences in egg size, we corre-
ARDEA 107(3), 2019
294
Verhoeven et al.: VARIATION IN EGG SIZE OF BLACK-TAILED GODWITS
lated egg size with wintering location. We obtained
wintering location in two ways. First, like Kentie et al.
(2017), we used resightings to classify individuals as
wintering south of the Sahara if they were seen in West
Africa at least once during the nonbreeding period
(July–March) in the years 2004–2017; we classified an
individual as wintering north of the Sahara if it was
resighted on the Iberian Peninsula in October during
the years 2007–2017. Second, we used geolocators
(Migrate Technology Ltd, Cambridge, U.K.) to deter-
mine whether females wintered north or south of the
Sahara. Using package ‘FLightR’ (Rakhimberdiev et al.
2017), we analysed the light-level data obtained from
37 females carrying geolocators (2012–2017). A detail -
ed example of this analytical method in Godwits can be
found in Rakhimberdiev et al. (2016). Eighteen of these
geolocator-carrying females were also assigned a
wintering location on the basis of resightings, and in 17
cases the two different methods led to the same result.
However, one individual was incorrectly assigned a
wintering location north of the Sahara based on the
resighting method; the geolocator data showed that at
the time of the faulty resighting, the bird was actually
south of the Sahara. We have also observed that of 36
geolocator-carrying females that crossed the Sahara in
2012–2018, two returned north to the Iberian Penin -
sula before the end of October (unpubl. data). As such,
some birds resighted on the Iberian Peninsula in
October and classified as wintering north of the Sahara
may in fact have migrated all the way to wintering
grounds south of the Sahara and already travelled
north again. In the present study, eight individuals were
resighted both north and south of the Sahara either in
the same winter (n= 4) or in different winters (n= 4)
and were thus assigned both wintering locations by the
resighting method. However, we are confident that
these cases were the result of the errors and limitations
of the resighting method described above, and we
have therefore excluded these eight individuals from
our analysis. It is highly likely that our sample still
includes some unidentified resighting errors of this
type, and these results should therefore be interpreted
with care.
(6) Sexual size dimorphism: Adult female Godwits
are 10–20% bigger than male Godwits (Schroeder et al.
2009) and Godwits have sexually specific growth rates
(Loonstra et al. 2018). We hypothesized that this sexual
size dimorphism might already be present in eggs, with
larger eggs containing females and storing more nutri-
ents than smaller eggs containing males. We therefore
related the genetic sex of the chick that hatched from
an egg to the size of that egg (continuous covariate)
using a generalised linear mixed model (GLMM) with a
binomial error distribution, a logistic link function, and
clutch included as random intercept.
(7) Hatching success: We used a GLMM with a
binomial error distribution and a logistic link function
to analyse whether the hatching success of a clutch
depended on its average egg volume, lay date, clutch
size or the age of the nest in days when it was found
(all continuous covariates). To make the intercept of
this model more meaningful, we scaled all these contin-
uous covariates by subtracting the mean and dividing
by the standard deviation. The random intercepts were
year and polder. The hatching success of a clutch is
determined by whether or not at least one egg hatches.
We were not able to model the number of hatched eggs
as a proportion of the total because we often arrived at
nests when only some of the eggs had hatched or after
the chicks had already left the nest. Because the chance
that a nest hatches is larger when a nest is found closer
to hatching, we included the age of the nest when it
was found, i.e. the number of days the nest was already
incubated when it was first discovered, as a covariate.
(8) Fledging success: We used a GLMM with a bino-
mial error distribution and a logistic link function to
analyse whether the fledging success of a clutch – the
number of chicks that survived in relation to the
number that were marked – depended on its average
egg volume or lay date (both scaled continuous covari-
ates). The random intercepts were year and polder. A
chick was considered to have fledged if it was resighted
35 or more days after being marked in the nest.
RESULTS
(1) There is considerable variation in the egg size of
our Godwit population (Figure 1). The global model –
the model with the largest sample size (Table 1) –
showed that egg size decreases with lay date and
increases with clutch size, but does not relate to nesting
attempt (Table 2). In this analysis, the time between
the first and the last egg in a year varied from 32–55
days, which means that over the entire season egg size
declined between 1.6–2.8%. The proportion of variance
explained by the fixed effects in this model was 0.004
(CI = 0.002–0.01). The adjusted repeatabilities from
this model were for individual: 0.60 (CI = 0.57–0.63),
clutch: 0.12 (CI = 0.10–0.14), year: 0.008 (CI =
0.001–0.02) and polder: 0.003 (CI = 0–0.01). As a
result, the residual variance – the proportion of vari-
ance attributed to undiscovered differences within indi-
viduals – was 0.27 (CI = 0.25–0.29).
295
(2) Heavier and larger females lay larger eggs; egg
size was positively correlated with both body mass
during incubation and the first principal component of
the linear measurements (Table 2). The proportion of
variance explained by the fixed effects in this model
was 0.06 (CI = 0.04–0.09).
(3) In the age model that included body mass and
structural size, the average egg size increased with age
(
b
= 0.52 ± 0.63, P= 0.002; Table 2, Figure 2) and
body mass was again a significant predictor of the vari-
ation in egg size (Table 2). The proportion of variance
explained by the fixed effects in this model was 0.18
(CI = 0.08–0.35). (3B) In the age model with a larger
dataset that did not exclude birds for which body mass
and structural size were missing, the average egg size
also increased with age (
b
= 1.99 ± 0.37, P< 0.001;
Table 2), but the slope of this increase decreased with
every additional year of age as identified by the signifi-
cant quadratic term (
b
= –0.18 ± 0.04, P< 0.001;
Table 2, Figure 2). The proportion of variance explain ed
by the fixed effects in this model was 0.12 (CI =
0.06–0.20).
(4) The relationship between egg volumes of
daughters and mothers was different between the two
age groups (
b
≤
2 years = 0.02 ± 0.19 vs.
b
≥
3 years = 0.38
± 0.23; Figure 3B), but not significantly so (F1,55 =
2.47, P= 0.12). We therefore averaged the egg volumes
of daughters across all their ages; this average was
significantly related to the average egg volume of their
ARDEA 107(3), 2019
296
0
2000
4000
6000
8000
30 40 50
volume (cm
3
)
count
Figure 1. Frequency distribution of 25,148 egg sizes measured
in southwest Friesland between 2004–2018. Three eggs with a
volume larger than 55 cm3(55.04 cm3, 55.11 cm3and 62.68
cm3, respectively), are omitted from this figure for graphical
purposes.
30
35
40
50
45
1
2
3
4
5
6
7
8
9
age
volume (cm
3
)
Figure 2. The relationship between egg volume and age for
Godwits in southwest Friesland. This graph shows the raw data
used in the analysis with body condition included (Model 3,
orange dots) and without body condition included (Model 3B,
orange + black dots combined). It also shows the modelled esti-
mates and standard errors from Model 3 (orange line, linear
relationship) and Model 3B (black line, quadratic relationship).
Model Eggs Volume Clutches Individuals Years Polders
(1) Global Model 5866 40.46 ± 3.23 1554 840 14 58
(2) Condition Model 3486 40.45 ± 3.24 925 756 14 57
(3) Age Model with 203 39.48 ± 2.81 53 40 9 21
(3B) Age Model without 504 39.84 ± 2.97 134 80 9 35
(4) Daughter ~ Mother – 39.13 ± 2.12 49 98a––
(5) Wintering Model 1099 40.07 ± 3.24 286 207 14 48
(6) Sexual size dimorphism 148 40.09 ± 3.21 99 –––
(7) Hatching success – 40.28 ± 2.88 6328 – 14 61
(8) Fledging success – 40.36 ± 2.80 1823 5265a9 61
Table 1. The number, mean size and standard deviation of eggs included in the different models. Also shown are the sample sizes for
the different grouping factors in each analysis. When the number of eggs is not given, the average egg size of the clutch was used in
the analysis. aIn these cases, ‘Individuals’ was not included as a grouping factor, but the entry still shows how many individuals were
part of the analysis.
Verhoeven et al.: VARIATION IN EGG SIZE OF BLACK-TAILED GODWITS
mothers (F1,47 = 6.83, P= 0.012; Figure 3C). The slope
of this relationship was 0.32 ± 0.12, and the herita bility
of egg size is therefore estimated to be 0.64 ± 0.24.
(5) The egg size of females that crossed the Sahara
was on average 3% smaller than the egg size of females
that did not cross the Sahara. Body mass was also a
significant predictor of the variation in the egg size of
this sample (Table 2). The proportion of variance
explained by the fixed effects in this model was 0.15
(CI = 0.09–0.22).
(6, 7 and 8) The genetic sex of a chick was not
correlated with the size of the egg from which it
hatched (Table 2). Our exploratory analysis of the fit -
ness consequences of egg size indicated that the chance
of hatching increased with larger average egg volume
and declined with lay date (Table 2). The chance that a
marked hatchling survived to fledging was not depen -
dent on the average egg volume of the clutch, but
declined with lay date (Table 2).
DISCUSSION
We observed considerable variation in the egg size of
Continental Black-tailed Godwits and investigated
which individual and environmental factors might
contribute to this variation. We also explored whether
this variation in egg size was associated with reproduc-
tive success. Approximately 60% of the observed varia-
tion in egg size was due to different individual Godwits
laying differently sized eggs, and only 27% of the
observed variation was the result of variation within
females across years. Consequently, we found that indi-
vidual factors such as female size, mass, age and
wintering location explained more of the variation in
egg size than did environmental factors such as year,
polder or lay date. Although we found egg size to be
heritable (h2= 0.64 ± 0.24), the actual individual
traits that underlie this heritable variation among indi-
viduals remain mostly undetermined. Finally, clutches
with larger eggs did, on average, have a slightly higher
chance of hatching, but chicks that hatched from larger
eggs were not more likely to fledge than chicks that
hatched from smaller eggs.
Environmental factors: annual, seasonal and local
variation
Both year and lay date explained a small amount of the
variation in egg size. These annual and seasonal
changes in egg size could be the result of differences in
both environmental and individual factors, such as the
temperature during egg laying and the age of females
(Robertson 1995, Hipfner et al. 1997). The seasonal
decline in egg size could also be an adaptive response
to the environment if laying smaller eggs earlier is more
beneficial than laying larger eggs later (Winkler & Allen
1996). Because the seasonal decline in egg size remains
present (though non-significant) when body mass,
structural size and age are included in the model (Table
2, models 2 and 3), we can infer that these factors are
likely not the cause of the seasonal decline. In any case,
since we did not find that second attempts were smaller
297
C
B
32.5
35.0
37.5
40.0
42.5
45.0
35.0
37.5
40.0
42.5
45.0
average volume of the maternal nest (cm
3
)
average volume of the daughter's nest (cm
3
)
A
35.0
37.5
40.0
42.5
45.0
35.0
37.5
40.0
42.5
45.0
1
age
2
3
4
5
6
7
8
9
<=2
age
>=3
Figure 3. The relationship between average egg volume of the maternal nest and average egg volume of the daughter’s nest, with
average egg volume of the daughters (A) given at each age for every daughter, (B) averaged into two different age categories for
every daughter, and (C) averaged for each daughter across her attempts at all ages. Heritability is estimated from relationship (C): Y
= 26.07 + 0.32 ×X, R2= 0.11, n= 49.
than first attempts nor that polders differed consis-
tently in egg size, we have no real indication that egg
size is influenced by environmental factors. This idea is
consistent with the outcome of food supplementation
experiments, which usually result in advanced lay dates
and larger clutch sizes but not in larger eggs (see
Christians 2002 for a review, and Ruffino et al. 2014 for
a meta-analysis).
Individual factors: wintering location, size, mass,
age, identity and reproductive performance
On the basis of resightings and geolocator data, indi-
vidual females wintering north of the Sahara laid on
average 3% larger eggs, which was also found by
Kentie et al. (2017). Body mass, structural size and lay
date were included in this analysis and are therefore
not the factors that explain the difference between
wintering locations. If disproportionally more young
birds were found to winter south of the Sahara than
north of the Sahara, we would speculate that the differ-
ence between wintering locations is the result of differ-
ences in female ages, but currently we are at a loss to
explain this difference in egg size between wintering
locations. Perhaps the longer migration itself results in
a decrease in egg size. If this were the case, individuals
from the same breeding location would differ in migra-
ARDEA 107(3), 2019
298
(1) Global Model
Fixed effects Estimate SE c2P
Intercept 39.41 0.62
Lay date –0.02 0.01 10.00 0.002
Clutch size 0.34 0.13 6.43 0.011
Attempt (2nd) 0.38 0.40 0.97 0.617
Attempt (unknown) 0.09 0.33 ––
Random effects Variance RSE
Clutch 1.23 0.12 0.01
Individual 6.32 0.60 0.02
Year 0.08 0.01 0.01
Polder 0.04 0.00 0.01
Residual 2.85 0.27 0.01
Table 2. The fixed effect coefficients and random effect variances of all models. The numbers and names correspond to those used
throughout the manuscript. We obtained chi-squared values for the significance of the fixed effects from likelihood ratio tests of
nested models with and without the variable of interest. Model 1 also shows the estimated adjusted repeatabilities.
(2) Condition Model
Fixed effects Estimate SE c2P
Intercept 38.23 0.83
Lay date –0.02 0.01 3.18 0.074
Clutch size 0.65 0.21 9.81 0.002
Body Mass (scaled) 0.57 0.09 38.68 0.000
PC1 0.15 0.06 5.09 0.024
Random effects Variance
Clutch 0.79
Individual 6.16
Year 0.00
Polder 0.02
Residual 2.78
(3) Age Model
Fixed effects Estimate SE c2P
Intercept 36.17 2.55
Lay date –0.03 0.03 1.02 0.313
Clutch size 0.52 0.63 0.84 0.359
Body Mass (scaled) 0.73 0.34 4.87 0.027
PC1 -0.16 0.24 0.41 0.523
Age 0.52 0.17 9.36 0.002
Random effects Variance
Clutch 0.05
Individual 3.67
Year 0.36
Polder 0.00
Residual 2.51
(3b) Age Model without condition
Fixed effects Estimate SE c2P
Intercept 34.23 1.52
Lay date 0.003 0.02 0.02 0.882
Clutch size 0.24 0.33 0.55 0.460
Age 2.15 0.37 27.91 0.000
Age2–0.20 0.04 21.66 0.000
Random effects Variance
Clutch 0.93
Individual 3.28
Year 0.11
Polder 1.28
Residual 2.74
Verhoeven et al.: VARIATION IN EGG SIZE OF BLACK-TAILED GODWITS
tory distance, and that difference in migratory distance
itself – independent of body condition – would be
related to differences in egg size. We have not found
any examples in birds to support this idea, but in the
migratory Chinook Salmon Oncorhynchus tshawytscha,
individuals migrating longer distances laid smaller eggs
than did individuals from the same breeding location
that migrated shorter distances (Kinnison et al. 2001).
Previous research on Godwits has hypothesized that
female Godwits vary the size of their eggs between
years to adjust to their endogenous condition
(Schroeder et al. 2009, 2012, Lourenço et al. 2011). We
found that approximately 5% of the total variation in
egg size observed across the population was explained
by differences in female body mass and structural size,
which indicates that in Godwits only minor adjust-
ments in egg size are associated with body mass.
However, we measured differences in body mass at the
end of incubation, which might not necessarily reflect
the differences in body mass during egg laying. Pick et
al. (2016a) found in an artificial selection experiment
with Japanese quail that the difference in egg size
between the study’s selection lines was mainly driven
by a differential increase in reproductive organ mass,
which was independent of body size. We can draw
three important conclusions from these findings: (1)
some variation in egg size is explained by the size of
the reproductive organs, (2) this is mostly independent
of female size, just as has been found in the present
study and other correlative studies on body size, and
(3) a change in body mass before or during the laying
period is potentially a good predictor of egg size,
whereas body mass during incubation – which is what
we measured – is likely less reliable. Regardless, our
299
Table 2. Continued.
(4) Daughter-mother relation
Fixed effects Estimate SE tP
Intercept 26.07 5.01
Egg volume mother 0.32 0.12 2.61 0.012
(5) Wintering Model
Fixed effects Estimate SE c2P
Intercept 38.50 1.53
Lay date –0.01 0.01 0.54 0.461
Clutch size 0.64 0.38 2.89 0.089
Body Mass (scaled) 0.86 0.16 25.73 0.000
PC1 0.18 0.12 2.27 0.132
Sahara (South) –1.13 0.36 9.49 0.002
Random effects Variance
Clutch 0.74
Individual 4.86
Year 0.32
Polder 0.47
Residual 2.44
(7) Hatching success
Fixed effects Estimate SE c2P
Intercept 0.21 0.14
Lay date –0.35 0.03 144.58 0.000
Clutch size 0.24 0.03 67.98 0.000
Average volume 0.06 0.03 4.84 0.028
Nest Age 0.59 0.03 373.41 0.000
Random effects Variance
Year 0.13
Polder 0.47
(6) Sexual size dimorphism
Fixed effects Estimate SE c2P
Intercept –0.05 0.16
Egg volume (scaled) 0.06 0.17 0.14 0.705
Random effects Variance
Clutch 0.00
(8) Fledging success
Fixed effects Estimate SE c2P
Intercept –2.01 0.21
Lay date –0.37 0.05 67.49 0.000
Average volume 0.01 0.04 0.03 0.855
Random effects Variance
Year 0.34
Polder 0.06
finding that body mass and size explain only a small
amount of the variation in egg size is similar to the
results previously published on other species (reviewed
in Christians 2002). It is also consistent with the high
repeatability of egg size in other avian species with
invariant clutch size, such as other shorebirds (e.g.
Väisänen et al. 1972, Nol et al. 1997, Dittmann &
Hötker 2001) and species with one-egg clutches
(Christians 2002).
We found that the egg size of Godwits increases
with age and that there is a significant relationship
between the average egg size of a mother and that of
her daughter. Both the increase in egg size with age
and the heritability of egg size are commonly found in
studies of avian egg size (reviewed in Christians 2002
and Williams 2012). Using the larger dataset of known-
age females we found a quadratic relationship between
egg size and age (Figure 2), which suggests that a
female’s egg size increases relatively more during her
first attempts and remains more stable later on. In addi-
tion, the relationship between daughters and mothers
becomes most apparent when the daughters are three
years old or older (Figure 3A, 3B). Both of these
patterns, as well as the high individual repeatability of
egg size, suggest that Godwits mostly increase their egg
size during their first two years of breeding and attain
their final egg size in the third year of breeding.
However, given the knowledge that some Godwits
breed in their first year while others defer breeding by
one or maybe even two years (Kentie et al. 2014), an
alternative explanation is that Godwits lay smaller eggs
only during their first attempt. The increase in egg size
during the first three years could simply reflect that the
proportion of females laying for the first time decreases
every year during that period, because of deferred
breeding. In any case, these results suggest that the
factors determining avian egg size partly develop with
age and are inherited.
The absence of a relationship between egg size and
the genetic sex of a chick might not be very surprising.
As the meta-analysis of egg sexual size dimorphism in
birds by Rutkowska et al. (2013) shows, there is very
little evidence for such a relationship across avian
species. We did find that smaller eggs had a slightly
lower chance of hatching. A potential reason for this is
that younger females tend to lay smaller eggs, and
younger females might also be less experienced and
therefore of lower quality in their execution of reproduc-
tive
activities such as choosing a nest site or defending
their nests against predators. It is also possible that
larger eggs inherently have a higher chance of
hatching. However, in the period from 2015–2017, we
collected 216 eggs from 40 clutches within our study
area and incubated them in an incubator (Loonstra et
al. unpubl. data); the hatching success of these eggs
was independent of egg size (binomial GLMM:
b
=
0.16 ± 0.23, c21= 0.49, P= 0.49). We therefore
believe that there is no inherent relationship between
hatching success and egg size. This same conclusion
was drawn from a cross-fostering experiment in the
ecologically similar Northern Lap wing Vanellus vanellus
(Blomqvist et al. 1997).
Egg size did not correlate with chick survival. This
corresponds to the lack of support for this relationship
in reviews by Williams (1994, 2005, 2012), but
contrasts with the more formal meta-analysis done by
Krist (2011); in the latter, egg size was positively
related to most studied offspring traits and the survival
of the chicks. One possibility for the lack of an effect of
egg size on chick survival in our study is that chick
survival is presently so low for Godwits that the orig-
inal benefit of larger eggs can no longer be observed
(Loonstra et al. 2019).
Lay date did influence both nest and chick survival:
earlier clutches had a higher chance of hatching and
fledging a chick. Previous studies have frequently
connected this decline in hatching success with the
seasonality of agricultural activities and predation pres-
sure (Kleijn et al. 2010, Schroeder et al. 2012, Kentie et
al. 2015). The seasonal decrease in fledging success
was also observed by Kentie et al. (2018) and might be
related to the seasonal decrease in body condition of
chicks (Loonstra et al. 2018). In any case, the mecha-
nisms underlying these survival patterns remain poorly
understood.
Conclusion
Even though Godwits have precocial chicks and an
invariant clutch size, our findings are strikingly similar
to results previously published on other avian species
(reviewed in Christians 2002). This is true of the
amount of variation in egg size, the degree of repeata-
bility and our inability to explain more than a small
fraction of the observed variation with either individual
or environmental factors. The high individual repeata-
bility of egg size across all of these studies indicates
that most birds do not adjust their total parental effort
to exogenous or endogenous conditions by varying
their egg size. Both nest and chick survival are nega-
tively correlated with lay date (Kentie et al. 2018, this
study) and the differences in lay dates within and
among females might therefore be a better indicator of
female condition.
ARDEA 107(3), 2019
300
Verhoeven et al.: VARIATION IN EGG SIZE OF BLACK-TAILED GODWITS 301
ACKNOWLEDGEMENTS
We thank the members of our field crews and many students
and volunteers for their help with collecting the data. We thank
Julie Thumloup, Marco van der Velde and Yvonne Verkuil for
their help with molecular sexing. This manuscript and the
authors benefitted considerably from the help of two critical yet
constructive anonymous reviewers. We are grateful to many
farmers, most of whom are organized in the Collectief Súdwest -
kust, and to the conservation management organizations It
Fryske Gea and Staatsbosbeheer for cooperation and granting
us access to their properties. The long-term Godwit research was
funded by the ‘Kenniskring weidevogels’ of the former Ministry
of Agriculture, Nature Management and Food Safety (2007–
2010, 2012, 2016), and the Province of Fryslân (2013–2017),
with additional financial support of the Prins Bernhard Cultuur -
fonds (through It Fryske Gea), the Van der Hucht de Beukelaar
Stichting, the Paul and Louise Cook Endowment Ltd., the
University of Groningen, BirdLife Nether lands and WWF-
Netherlands. Funding for this manuscript was provided by the
Spinoza Premium 2014 of the Netherlands Organisation for
Scientific Research (NWO) awarded to TP. This research was
conducted under license numbers 4112B, 4339E, 6350A follo-
wing the Dutch Animal Welfare Act Articles 9 and 11.
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SAMENVATTING
Net als bij de meeste vogelsoorten is er ook bij Nederlandse
Grutto’s Limosa l. limosa veel verschil in eigrootte. Die variatie is
vooral het resultaat van verschillen tussen individuen. De indivi-
duele verschillen zijn consistent tussen jaren. Een vergelijking
van de eigrootte van dochters met die van hun moeder sugge-
reert dat een deel van deze individuele variatie erfelijk is.
Daarnaast kan ongeveer 5% van de variatie tussen individuen
worden verklaard door verschillen in lichaamsgewicht en
lichaamsgrootte van het vrouwtje. Minder dan 1% wordt ver -
klaard door de legdatum, het jaar en de nestlocatie. Het over-
grote deel van de variatie in eigrootte tussen individuen blijft
daarom onverklaard. De afwezigheid van duidelijke verschillen
in eigrootte tussen jaren, binnen jaren en tussen locaties, maar
ook de afwezigheid van een sterke relatie met lichaamsconditie
maken het onwaarschijnlijk dat de eigrootte een afspiegeling is
van de conditie waarin het vrouwtje zich bevindt op het
moment waarop de eieren worden gelegd. Toch vonden we dat
oudere vrouwtjes grotere eieren leggen dan jongere vrouwtjes,
wat erop zou kunnen wijzen dat er aan leeftijd gerelateerde
verschillen zijn in de conditie waarin vrouwtjes verkeren op het
moment van het leggen van de eieren. Alhoewel vrouwtjes de
grotere sekse zijn, wordt geen van de variatie in eigrootte
verklaard door het geslacht van het kuiken dat uit het ei komt.
Nesten met kleinere eieren hebben een iets kleinere kans om uit
te komen, maar de eigrootte is niet gerelateerd aan de kuiken-
overleving. De legdatum is daarentegen wel sterk gerelateerd
aan de nest- en kuikenoverleving. Het is daarom mogelijk dat
voor Grutto’s de legdatum een betere afspiegeling is van de
conditie waarin het vrouwtje zich bevindt op het moment van
leggen dan de grootte van de eieren die ze legt. Deze suggestie
is mogelijk algemeen voor vogels, omdat bij voeren van vogels
voorafgaand aan het leggen van de eieren meestal resulteert in
een vervroeging van de legdatum of een vergroting van de
legselgrootte, maar niet in grotere eieren.
Corresponding editor: Sjouke Kingma
Received 7 February 2019; accepted 9 October 2019
