453
T h e Influence of Laying Sequence and Ambient Temperature
on Egg Size Variation in the Swallow Hirundo rustica
Jerzy Bafibura and Piotr Zielifiski
BA~ZmURA,J., & ZIELIIqSKI,P. (1995): The influence of laying sequence and
ambient temperature on egg size variation in the Swallow Hirundo
rustica. J. Orn. 136: 453-460. - Intra-clutch egg size variation was studied in
SwallowsHirundo rustica in central Poland during two breeding seasons differing
very much with respect to weather conditions. No correlation between egg
volumes, lengths or breadths and the egg laying order was found. In one season
(with high mean temperature and low precipitation) the final egg tended to be
larger than the mean size of the preceding eggs in the clutch. Such a difference
was not observed in the other season (with low mean temperature and high
precipitation). This fact seemed to be connected with a general impact of weather
conditions prevailing in each year on the breeding ecology of Swallows. There
was no evidence for an expected short-term effect of temperature on egg size. All
this suggests that the relation between proximate and ultimate factors affecting
egg size variation may be very complex.
Department of Ecology and Vertebrate Zoology, University of L6d~, Banacha
12/16, 90-237 L6d~, Poland
Introduction
Within-clutch variation in egg size has been explained in both ultimate (SLAcSVOLDet
al. 1984) and proximate (JaRvINEN & YHMA~U 1986) terms. There is ample
evidence, observational and experimental, for the adaptive value of patterns connected
with hying sequences in some species (e g. Howe 1976). On the other hand, the
operation of proximate constraints seems to better explain other observed patterns
(SLAGSVOLD&5 LIFJELD1989).
On the basis of an unpublished data set of SLAGSVOLDet al. (1984) classified the
Swallow Hirundo rustica as a species employing the brood survival strategy characterized by the final egg in the clutch being larger than the mean egg size for the entire
clutch. As far as we know, there are no other published data on intra-clutch variation
of egg size in this species. No data on the influence of any meteorological variables
on egg size in the Swallow have so far been published either. Ambient temperature
could potentially affect egg size by means of influencing the female physiology and/or
the abundance of flying insects constituting almost the exclusive food of Swallows.
In this paper we present data on intra-clutch egg size variation in the Swallow in two
breeding seasons varying very much in weather conditions. We examine the data
to find out if there is any consistent pattern in this variation; we especially focus
our attention on the relative size of the final egg. We also analyse the influence of
temperature on egg size
454
Journal fhr Ornithologie 136, 1995
Materials and Methods
Egg characteristics were recorded for this study at farms located in central Poland near the
village of Ktery (52 o 15' N; 19 ° 25' E) from June to September 1981 (22 clutches) and at
Go~lub (52 o 05' N; 19 ° 28' E) from May to September 1994 (21 clutches). All clutches studied
in 1981 were repeat or second clutches (late clutches). In 1994, we studied both first clutches
(early clutches) and repeat and second clutches (late clutches).
In a sample of clutches the subsequent eggs were measured on the day of laying, resulting
in complete information about the laying sequences (8 clutches in 1981 and 4 in 1994). Information about other clutches was less complete; at least the first egg was identified in 14 clutches in 1981 and in 13 clutches in 1994, and at least the ultimate egg was identified in 18 and
21 clutches in 1981 and 1994, respectively.
We measured the length (L) and breadth (B) of eggs to the nearest 0.1 mm with a sliding
caliper and estimated volume after MANNING(1979) using the formula
V = 0 . 5 0 7 x L x B 2.
Where indicated in the text, egg characters were expressed as intra-clutch standard deviates or
z-scores, i. e. the deviations of the measurements of particular eggs from the respective clutch
means divided by the within-clutch standard deviation. Adult birds were caught in mist nets,
ringed, measured and released (procedure described in BA~BURA 1986). Statistical procedures
were used following SOKAL& ROHLF (1981) and ZAR (1984).
Meteorological data were obtained from the meteorological stations Blonie (1981) and
Bor6w (1994).
We thank members of the Students' Ornithological Club, L6d{ University, for assistance in the field in
1981. We are grateful to H. WAgSZAWSKr,the Director of the Stadnina Koni Walewice Ltd. for his permission to study swallows at the Go~lub farm. The study was supported by a grant PB 6/P205/169/04 from
the KBN. We thank L. GLOWACKIfor correcting the language of this paper.
Results
Different clutches show a high degree of variation in egg size in relation to the laying
sequence, so that no clear pattern appears (Fig. 1). As different internal and external
factors can obscure a potential pattern, we examined in detail the egg sequences in four
1981 clutches of the same size (5 eggs), laid at exactly the same time (Fig. 1). The eggs
in these sequences were not significantly concordant with respect to any trait (Kendali's coefficient of concordance: W = 0.322; W = 0.244; W = 0.422 for egg volume,
length and breadth, respectively). The correlation between the egg characteristics in
these clutches and the laying order was not significantly different from zero (r = 0.135;
r = 0.288; r = --0.057 for volume, length and breadth, respectively). Consequently,
there is no evidence for any c o m m o n factor influencing sequence-related egg size variation in different clutches.
In spite of the lack of an overall laying-order-related pattern of within-clutch variation in egg characteristics, a special relation could still be expected between the size
of the ultimate egg and the average size of the preceding eggs within clutches; ultimate
eggs would be expected to be bigger than the respective means for preceding eggs, and,
as a consequence, clutch means. The ultimate egg was indeed bigger (size expressed as
z-scores, ZAg, 1984) than the preceding ones in 1994, but not in 1981 (Table 1,
J. BAS,r~URA & P. ZIELIIqSKI:Egg size variation in Hirundo rustica
455
Fig. 2). In 1994, the difference for first clutches was not significant, but it was significant in late clutches and pooled early and late clutches (Table 1). This suggests that
in at least some years ultimate eggs tend to be greater than mean of the remaining ones.
In no year was there any significant correlation between clutch mean egg lengths,
breadths and volumes and mean daily temperature on six days before the start of
laying, neither was there any correlation between these egg traits and the average
temperature over the six-day period, the early and late 1994 clutches being analysed
both separately and pooled (84 correlation coefficients ranged from --0.53 to 0.33, 46
coefficients negative and 38 positive).
We also analysed correlations of volumes, lengths and breadths of the first and
ultimate eggs standardized within clutches (z-scores) with mean daily temperature on
each of six days preceding the laying of these eggs. Only 5 out of 126 correlations
(ranged from --0.71 to 0.79, 58 coefficients negative and 68 positive) were significant
at the 0.05 level (Table 2). Taking into consideration the non-independence of individual correlations and the resulting high overall error rate, there is very weak
evidence for any influence of ambient temperature on the observed egg size variation.
2150 •
2200
2100 •
\
2050"
~- 2 0 0 0
2000
,t,,, ~
~ 1950
&
//.+ x,\\
x
E
. .'''"'
. ,/'"" i ,A-[;'\\:'~,
1900.
E
=
1900
1800
1850
u~ 1 8 0 0
1700
\
1750
1600
1700
1650
.!
>t
2500
2400
2300
E
u
2200
~ 2100
=
............................
~:~::+~_
::i[.
2000
1900
Fig. 1. Examplesof variationin egg volume in
individual laying sequences in 1981 and 1994.
Four out of five 5-eggclutchesin the top figure
were laid at the same tim~
,,. . . .
1800
~o"
./
1700
1600
1
2
2
4
Order of laying
5
6
456
Journal fiir Ornithologie 136, 1995
Tab. 1. The t-test of differences between paired lengths (L), breadths (B) and volumes (V)
of ultimate eggs (u) versus mean values for the preceding eggs (m). The one-tailed test, Ho:
m
=>u v. Ha: m
<u.
Year (clutch)
L
t-values for:
B
V
1981
(late clutches)
--1.30
df = 17
P >0.1
1.41
df = 7
P >0.1
2.61
df = 12
P <0.025
2.99
df = 20
P <0.005
1.12
df = 17
P >0.1
0.71
df = 7
P >0.1
2.46
df = 12
P <0.025
2.07
df = 20
P <0.O5
0.14
df = 17
P >0.1
1.08
df = 7
P >0.1
2.88
df = 12
P <0.01
2.80
df = 20
P <0.025
1994
(early clutches)
1994
(late clutches)
1994
(pooled)
Discussion
For many species of birds a more or less clear within-clutch pattern of the layingsequence-related variation in egg size has been observed, egg size being increasing
(e. g. HOWE 1976, WINr~L 1970, BRYANT 1978, RYDEN 1978, ZACH 1982, HAFTORN
1986, LOWTHeR1990, WIGGINS 1990, POTTI 1993) or decreasing with each sequence (e.
g. BANCROFT1984, ROFSTAD& SANDVIK1985, ARNOLD 1991, ROBERTSON& COOKE
1993, JOVER et al. 1993). In some cases no egg size relation with the laying sequence
or a non-linear pattern has been recorded (e. g. O]ANEN et al. 1981, GREIG-SMITHet
al. 1988, ARNOLD 1991).
Following HOWE (1976), CLARK & WILSON (1981) and SLAGSVOLDet al. (1984)
special attention has been focused on the adaptive significance of intra-clutch egg size
variability and, in particular, the significance of the size of the final egg. As the chick
size at the moment of hatching is known to correlate with egg size (see WII.LIAMS
1994 for review), this latter influences the initial size hierarchy amongst nestlings and,
as a consequence, may affect sibling competition between nestlings. SLAGSVOLDet al.
(1984) suggested that in birds there are two basic breeding strategies connected with
manipulating the competitive properties of nestlings. Birds adopting the brood reduction strategy lay a relatively small ultimate egg, while relatively big final eggs are laid
by birds adopting the brood survival strategy.
On the other hand, JARVINEN & YLIMAUNU(1986) argued that in at least some
species intra-clutch egg size variation does not have any strategic meaning. It rather
results from female susceptibility to weather conditions, so that in cold seasons or cold
periods within seasons females cannot afford the production of large final eggs. This
implies that the size of an individual egg, as measured by the deviation from the clutch
mean, should reflect weather conditions at critical time during its formation. So,
j. BAI"trBURA& P. ZIELIIqSKI:Egg
size variation in Hirundo rustica
457
proximate factors, energetic and nutritional conditions at the stage of egg formation,
were proposed to explain an increase in egg size with the laying sequence in Pied
Flycatchers Ficedula hypoleuca (SLAGSVOLD& LmJ~LD 1989).
However, these hypotheses do not seem to be mutually exclusive. The existence of
proximate constraints does not rule out the possibility that some patterns can have
ultimate significance. It is interesting that certain within-clutch patterns appear in some
seasons but not in others as it was the case in the Pied Flycatcher (JAttvr~zN &
YLIMAmNU 1986).
In the Swallow we observed no consistent tendency in sequence-related egg size variation, although the ultimate egg tended to be larger than the mean of the remaining
eggs in the dutch in one year (1994). In the other year of this study (1981) there was
0.80.6-
I Late clutches I
"~
..."" ,x
...,"'.i" ~,,i-
0.4-
:@
ili~.......
0.2-
..~;~i >.....
"o
o
~ ~.2-0.4-
x"[..-;S.....
-0.6-0.8
First iN=8)
Middle' (N=8)
Last (bl=l 3)
0.¢
0"5t
0.4
I Early and late clutches
I
t/'~
"
.l i
0.3
"~ 0.2
0.1
-0.1
J
-0.2
4).3
-0.4
First (h1=13)
I'--x-
Length
. Middle '(N=13)
Position in sequence
--+- Breadth ~
Last (b1=21)
Volume
I
I
Fig. 2. Means of standardized values (z-scores) of length, breadth and volume of first, middle, and ultimate
eggs for the 1994 late, and pooled early and late clutches. Unweighed clutch means of middle eggs (not
individual eggs) were treated as units.
458
Journal fiir Ornithologie 136, 1995
Tab. 2. Significant (P <0.05) coefficients of correlation between lengths, breadths and volumes of the ultimate eggs standardized within clutches and mean daily temperature on 6 days
preceding the day of their laying, t-n -- mean temperature on the n day before laying. Only
1994 season is presented as no significant correlations were found in 1981.
Clutch category
Variables
Correlation (dr)
early
early
early
early + late
early + late
t-1 v.
t-1 v.
t-4 v.
t-1 v.
t-2 v.
0.74 (6)
0.79 (6)
-0.71 (6)
0.43 (19)
0.46 (19)
breadth
volume
length
breadth
breadth
no difference These two years differed very much in respect to the weather (Table 3).
The 1981 breeding season was much colder and rainier than 1994. Because airborne
insects, the almost exclusive diet of the swallow, are very sensitive to rain and low
temperature, bad conditions in 1981 could impose more constraints on breeding
females, which could result in the lack of size difference between the ultimate egg and
the remaining ones. In contrast, in the breeding season of 1994 characterized by good
weather, the difference appeared as a result of a low level of constraints. Actually the
difference was significant for late clutches, i. e. at the time when conditions are
generally believed to progressively get worse. RYDEN (1978) observed an increase of
egg size with the laying sequence in early clutches of the Blackbird Turdus merula but
in late clutches there was no correlation.
Although general characteristics of breeding seasons seem likely to affect withinclutch egg size patterns, at least the relative size of final eggs, we were not able to find
the expected positive relationship between egg size and ambient temperature at the
time preceding egg laying. Such a relationship has been thought to be a result of the
negative influence of low temperature on oocyte growth during the fast growth stage,
3--5 days before laying (KENDEIGH1941, PINOWSKA1979, OJANEN 1983, JXRVlNEN &
YUMaUNU 1986, MAGRATH1992). One reason for the lack of this connection may be
the fact that female Swallows spend nights inside farm buildings (MoI.L~P, 1994,
TURNER 1994, own obs.) and thus are not directly exposed to lowest night temperatures. This could limit their effect on the female physiology.
To sum up, although in the Swallow the final egg seems to be larger than the clutch
mean value, at least in some seasons (this study, SI.AGSVOU)et al. 1984), there is no
evidence for any other consistent pattern of egg size variation connected with the
laying order. There is also little evidence for a marked short-term influence of ambient
temperature on the relative size of eggs within clutches. It is possible that temperature
works in concert with other environmental variables affecting the availability of food
and the female physiology. Even if such proximate factors are at work, the withinclutch aspect of egg size variability may still have adaptive significance. The possible
interrelations between proximate and ultimate factors may be very complex and
remain to be further investigated in Swallows.
j. BAI<~BURA& P. ZIELIIqSKI:Egg size variation in Hirundo rustica
459
Tab. 3. Mean monthly temperatures (°C) and sum of precipitation (in ram) during the 1981
and 1994 Swallow breeding seasons.
1981
1994
temperature
precipitation
temperature
precipitation
May
June
July
August
14.1
46.4
14.1
72.2
16.9
68.1
17.7
17.9
17.5
99.2
24.1
43.2
16.5
61.9
19.7
26.6
Zusammenfassung
In Zentalpolen wurde die Variation der Eidimensionen innerhalb eines Geleges bei der Rauchschwalbe in zwei Brutperioden untersucht. Die beiden Jahre unterschieden sich in den Witterungsverh~iknissen stark voneinander. Zwischen Eivolumen, -l?inge und -breite und der Legefolge wurden keine Korrelationen gefunden. In einer Brutsaison (hohe Mitteltemperaturen
und geringe Niederschl~ige) war das letzte Ei eines Geleges tendenzielll gr6t~er als das Mittel
der vorher gelegten Eier. Ein derartiger Unterschied lief~ sich in der anderen Brutsaison (niedrige Mitteltemperaturen, hohe Niederschl~ige) nicht feststellen. Dies scheint mit generellen
Folgewirkung des jeweils vorherrschenden Wetters zusammenzuh~ngen. Ein Kurzzeiteffekt
der Temperatur auf die Eigr6f~e lief~ sich wider Erwarten nicht nachweisen. Die Befunde
deuten an, daft fiir die Variation der Eigr6f~e verantwortlichen unmittelbaren und mittelbaren
Faktoren sehr komplex sind.
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