The Auk 121(1):103–109, 2004
MORE EGGS THE BETTER: EGG FORMATION
IN CAPTIVE BARN OWLS (TYTO ALBA)
J M. D
,1 S M
, Y H
Centre d’Écologie et Physiologie Énergétiques, Centre National de la Recherche Scientifique,
23 rue Becquerel, F-67087 Strasbourg Cedex 02, France
A.—We studied rapid yolk deposition (RYD) in Barn Owls (Tyto alba) on the basis of
the analysis of 26 eggs laid by “dye-dosed” captive female Barn Owls in five different broods.
Pictures of yolks were examined to assess daily rates of yolk deposition. We used those data
in combination with data from the dissection of ovaries of another five breeding females. We
found that the total duration between initiation of RYD and laying of the corresponding egg
was only 13.6 days, with an interval between yolk completion and oviposition of 2.4 days. The
total number of follicles that may have given eggs was found to be 25. That high number of
follicles and the short RYD period explain the particularly high reproductive potential of this
nocturnal raptor species. Received 22 January 2003, accepted 15 September 2003.
R.—Nous avons étudié le dépôt rapide du vitellus (DRV) chez Tyto alba. L’étude est
basée sur l’analyse de 26 œufs répartis en cinq couvées provenant de femelles de Tyto alba captives ayant ingéré des pigments lipophiles. Les photographies de vitellus ont été examinées pour
estimer les taux journaliers de dépôt en vitellus. Nous avons exploité ces données combinées à
d’autres issues de la dissection des ovaires de cinq autres femelles reproductrices. Nous avons
trouvé que la durée totale entre l’initiation du DRV et l’éclosion des œufs correspondant était
seulement de 13,6 jours, avec un intervalle de 2,4 jours entre l’achèvement de la formation du
vitellus et l’oviposition. Un total de 25 follicules se seraient développés pour donner des œufs.
Ce grand nombre de follicules et la courte durée de la période de DRV expliquent le potentiel
reproductif important de ce rapace nocturne.
R
breeding aempt
is one of the main parameters defining lifehistory strategies (Stearns 1992). In birds, the
yolk constitutes the major energy content of
an egg (Sotherland and Rahn 1987). An estimate of the daily amount of yolk deposited on
developing ova and the sequence of laying are
important when evaluating the total cost of egg
production. In birds, the vast majority of the yolk
mass is deposited in a relatively short period of
time compared to other oviparous vertebrates;
in some passerines, rapid yolk deposition (RYD)
may last only three days per yolk (Ricklefs 1974,
Grau 1984). During RYD, growing follicles take
up from the blood the yolk precursors that are
produced and secreted by the liver (Griffin and
Hermier 1988, Shen et al. 1993); follicle growth
occurs in a hierarchy with at most one follicle
reaching maturity and being ovulated each day
(Christians and Williams 2001).
1
Present address: Centre for Ecological and Evolutionary Synthesis, Division of Zoology, Department of
Biology, University of Oslo, P.O. Box 1050 Blindern, 0316
Oslo, Norway. E-mail: joel.durant@bio.uio.no
Clearly, the energy cost of egg production is
determined by clutch size and the variation in
rate of growth of follicles recruited, duration
of the follicles’ growth, or both. Even though
the energetic demands during clutch formation were modelled 30 years ago (King 1973),
and a technique is available to assess daily
energy–nutrient demands during yolk formation (Warren and Conrad 1939, Gilbert 1972,
Grau 1976), few studies have aempted to
empirically examine such demands in birds
(Astheimer and Grau 1985).
In birds that lay big clutches, total number of
eggs in formation (Haywood 1993) and laying
interval (Astheimer 1985) must be taken into account to estimate the daily yolk-deposition rate.
Moreover, the number of follicles that undergo
yolk deposition commonly exceeds number of
eggs actually laid (Meijer et al. 1989), which suggests that unlaid yolks become atretic (Erpino
1973, Gilbert et al. 1983). Thus, it is important
to take into account the actual number of eggs
laid, all eggs resorbed before oviposition, and
all the follicles that undergo atresia, when assessing the energy–nutrient requirements for an
entire reproductive aempt.
103
D
, M
, H
104
Among raptors, the Barn Owl (Tyto alba) has
an exceptionally high reproductive potential,
which is rather similar to that of passerine
birds. This owl species commonly lays clutches
of four to seven eggs (Taylor 1994), where clutch
size varies widely according to food availability
(Mikkola 1983, Taylor 1994). No accurate data
are available on the laying interval, ovary structure, and timing of yolk development in Barn
Owls. We predicted that the high reproductive
potential in this altricial species, associated with
a low daily energy requirement of egg synthesis
(Durant et al. 2000, Vézina and Williams 2002),
is due to a long RYD period and a possibility of
recruiting a larger number of follicles for RYD
than eggs actually laid.
The aim of our study was to characterize the
phases and timing of egg formation in captive
Barn Owls to understand the high potentiality
of laying in this species. Likewise, we also conducted an ovary analysis and determined the
number of developing follicles.
M
The study was performed on captive European
Barn Owls that were part of a breeding program
conducted since 1985 in our laboratory. Each pair of
owls was housed separately in an outside aviary (5 ×
4 × 2.5 m) where a nest box was available. They were
fed daily with laboratory mice (Mus musculus). Laying
takes place from March to October. The average egg
laying interval was 2.4 ± 0.5 days (n = 96) (i.e. laying
occurred at different times of the day for successive
eggs).
D
R Y D
Rapid yolk deposition is the deposition period
for lipoprotein yolk on the enlarging proteinaceous
primordial follicle. A lipophilic dye, Sudan black B,
was given orally and used as a date marker of the yolk
structure during follicle development (see Warren and
Conrad 1939, Gilbert 1972, Grau 1976 for techniques).
Because the yolk is laid down in layers by addition of
material to the outer margin (Gilbert 1979), the dye
ingestion results in a distinct ring within the yolk, the
deposition of that ring can be linked to the date of dye
ingestion.
The experiment was conducted on five captive
female Barn Owls. The average clutch size was 5.0 ±
0.4 eggs with a total of 26 eggs. Nests were checked
daily to see when the laying started. Just aer the laying of their first egg, females were fed with a gelatin
capsule containing 50 mg of dye and weighed. Birds
were thereaer dye fed every second day until the last
[Auk, Vol. 121
egg was laid. To minimize disturbance of breeding
birds, the gelatin capsule was put under the skin of
a freshly killed mouse (see Close et al. 1997 for procedure for small mammals). In the morning, the mouse
was substituted for the prey store created by the male
during the previous night inside the nest box. In the
aernoon, we checked that the mouse was eaten and
then put the prey store back into the nest. The average delay between deposition of the mouse with the
capsule in nest and its disappearance (i.e. its ingestion
by the female) was 6.6 h (0–10.5 h).
Freshly laid eggs (n = 26) were collected for dyering analysis and replaced immediately with dummy
eggs to prevent a possible prolongation of laying
(Haywood 1993). Eggs were measured (length and
breadth) with a caliper to the nearest 1.0 mm, weighed
to the nearest 0.01 g, and frozen at –15°C. Frozen eggs
were treated later following Grau (1976, 1996). They
were put into hot water (40°C) for a few seconds, shell
and membranes removed, and frozen contents fixed
in 4% formalin at 60°C for 16 h. Shells were dried at
60°C for 48 h and weighed.
Aer fixation, all albumen was removed; spherical
yolks were weighed, cut in half, and one half stained
with 6% potassium dichromate for 16 h at 60°C.
Enlarged slides were used to measure yolk radius,
to locate the position of the dyed yolk rings, and to
measure the relative thickness of each yolk layer delimited by dye. The slides allowed us to estimate the
daily yolk-growth increment (Astheimer and Grau
1990) and to calculate the duration of RYD.
Yolk deposition in birds follows a more-or-less
exponential curve (see Astheimer and Grau 1990 for a
review). To compare the RYD rate with an ANCOVA
(Zar 1984), we fied a linear equation aer logtransformation of the y-axis (yolk-deposition rate) to
each egg data-set with more than three dye rings (n =
9) . Among the five clutches, only one had several eggs
(n = 4) with more than three dye rings. That clutch was
used to analyze the potential effect of the laying order
on RYD rate.
O A
Ovaries of five other breeding females obtained
from another study (Durant et al. 2000) were used.
Fresh ovaries were weighed and dissected under a
binocular microscope. Five follicle types were distinguished (Los and Murton 1973): (1) RYD follicles
undergoing rapid yolk development; (2) primordial
follicles, which are small follicles not yet recruited
into a follicular hierarchy of RYD; (3) mature follicles; (4) postovulatory follicles, which are those
ruptured aer ovulation (remnant of a follicle whose
ovum was ovulated); and (5) atretic follicles, which
are the follicles that undergo atresia before ovulation.
To eliminate confusion between atretic and postovulatory follicles, those follicles were excised from the
January 2004]
Egg Formation in Captive Barn Owls
105
ovary and cut in half for examination of their internal
structures. A postovulatory follicle appears as a flat
yellow purse aached to the ovary by a large isthmus.
On the other hand, depending on the stage of atresia,
the cut atretic follicle has a dense zone surrounding
the visible oocyte containing a yolky residue or is
occluded. In a more advance stage, an atretic follicle is easily distinguished without examination of
its internal structure by its deformed or shrunken
appearance.
R
D
R Y D
The yolks (n = 26) measure on average 18.8 ±
0.1 mm (SE) for an average mass of 3.4 ± 0.1 g
(SE). Calculated average yolk density was 0.96 ±
0.01 cm3 (SE).
Because we started feeding dye to birds aer
the laying of the first egg, that first egg was
not used in the analysis of RYD. The secondlaid egg of all clutches studied did not show
dye rings, which meant that the yolk deposition was completed for those eggs at the time
of dye ingestion (i.e. laying of the first egg).
Consequently, the first egg marked with a dye
ring was always the third-laid egg. Each following egg had thereaer one more dye ring
than the preceding one.
The more peripheral dye ring observed in a
yolk (i.e. the most recently deposited dye ring)
corresponds to ingestion of pigment 2.4 days
before laying. The time period between the end
of RYD and oviposition is then >2.4 days. The
smaller and most central dye ring observed (i.e.
deposited nearest to the initiation of RYD) corresponds to pigment ingestion 13.6 days before
laying (fih dye ring). Thus, the RYD period
lasts 11.2 days.
We calculated the mass of the sphere delimited by each dye ring assuming that the
yolk is homogeneous and applying its density.
Cumulative yolk mass expressed as a function
of time is presented in Figure 1. The smallest
dye-ring diameter observed (3.7 mm) corresponded to 20% of the final yolk diameter and
weighed 0.03 g. The yolk enlargement rate was
on average 1.6 mm day–1.
Neither the laying order nor the different
clutches had an effect on the RYD (ANCOVA:
F = 0.76, df = 6 and 9, P > 0.25; and F = 2.38, df = 6
and 21, respectively). Consequently, we pooled
data from the different eggs and broods and
F. 1. Rate of Barn Owl egg-yolk deposition estimated by administration of lipophilic dye. The cumulative yolk growth is expressed as a percentage of
final yolk mass at egg laying. To the pooled data, we
fitted a second-order polynomial equation (see text):
y = 133.054 + 14.0375 × x + 0.29796 × x2 (F = 186.23,
df = 2 and 46, P < 0.001, r2 = 0.89), where y is the yolk
mass in percent and x is the number of days before
laying (Astheimer and Grau 1990). This equation is
valid only over the presented range of yolk mass (0
to 100%). Inset is a schematic showing the position of
the dye rings with their respective ages (sixth egg of
a clutch).
fied to them a second-order equation (Fig. 1)
that indicates that RYD started and stopped 13.2
and 2.5 days, respectively, before laying.
Using values for beginning and ending of
RYD, a timing of events could be drawn (Fig. 2).
O O A
The ovary structure presented numerous follicles at different stages of development (Table
1). Follicles with a mass <0.03 g (mass of the
inner yolk delimited by the smallest dye ring
obtained) were considered to be primordial follicles. The number of primordial follicles was 2×
higher than the clutch size. Follicles with a mass
exceeding 0.03 g were considered to have begun their RYD. Those RYD follicles were easily
identified by their yellow color and ovoid form.
Their mass and size were different according to
their stage of development. At the latest stage,
mature follicles, a stigma was visible, and the
follicles were suspended from the surface of
D
, M
, H
106
[Auk, Vol. 121
F. 2. Timing of egg development for a clutch of six eggs and two atretic follicles. Rapid yolk deposition
(RYD) was assumed to start 13.6 days before oviposition with and time period between the end of RYD and oviposition interval of 2.4 days. The delay between each RYD initiation was assumed to be equal to laying interval
(i.e. 2.4 days). The resorption of surplus yolk was assumed to begin after the laying of the last egg. The arrows
mark the moment of dye deposition inside the yolk.
the ovary by a narrow isthmus of tissue, the
pedicle.
Each postovulatory follicle corresponded to
an ovulated ovum; the smallest (i.e. oldest), visible postovulatory follicle corresponded to an
egg laid eight days before killing (the third of a
five-egg clutch, sacrifice taking place three days
aer the last laying).
Each ovary presented several atretic follicles.
We assumed that atretic follicles >0.03 g came
from RYD follicles that had failed to develop
further. Only those atretic follicles could have
given an egg and were considered (Table 1).
D
R Y D
This is the first time that the RYD duration
has been determined for Barn Owls and to our
knowledge only the second time for a raptor
species (Meijer et al. 1989). We determined that
RYD in Barn Owls starts 13.6 days before laying and lasts ~11 days. Barn Owls are known
to be able to lay replacement clutches, second
and third clutch (Taylor 1994). In the aviary, we
observed that the first egg of the replacement
TABLE 1. Summary analysis of ovaries.
Follicles
________________________________________________________________
Owl
A
B
C
D
E
Mean ± SE
a
Clutch size
7
7
4
5
8
6.2 ± 0.7
Primordial
14
6
12
18
19
13.8 ± 2.3
RYD
2
2
3
3
4
2.8 ± 0.4
Postovulatory
6
4
4
4
7
5.0 ± 0.6
Atretic
5
2
1
2
3
2.6 ± 0.7
Total = number of follicles that had or could have given an egg (i.e. clutch size + primordial + RYD + atretic follicles).
Total a
28
17
20
28
34
25 ± 3
January 2004]
Egg Formation in Captive Barn Owls
clutch could be laid as early as 14 days (n = 21)
aer the clutch removal. That value is consistent
with the time necessary to produce an egg, from
follicle recruitment to oviposition, and indicates
that the Barn Owl needs only 14 days to produce a second clutch.
Is RYD affected by the birds’ captivity? To our
knowledge, no study addresses that problem.
Obviously, a difference in diet could affect RYD.
However, the body mass increase of captive
and wild females during the prelaying period
is similar in duration and intensity (Durant
2000). In our study, all birds were fed ad libitum.
Such ad libitum feeding of the female during egg
synthesis is not uncommon in the wild. Indeed,
the male oen provides its nest-confined mate
an excess of prey, which accumulates in the nest
room (Taylor 1994, Durant et al. 1996, Durant
2000). The main prey of the European Barn Owl
during reproduction in eastern France is the
common vole (Microtus arvalis, Muller 1991),
which has a higher average caloric value than,
but a similar composition as, the laboratory
mice fed to our birds (7.74 and 6.6 kJ g–1, respectively; Wijnandts 1984, Durant et al. 2000). Thus,
it seems safe to assume that the diet provided in
the present study mimics the natural conditions
and that the RYD measured is representative of
the RYD in the field, or at least faster.
The Barn Owl RYD period has long been
compared to other altricial species (studied in
the wild and in captivity). For example, Rock
Pigeons (Columbia livia), which lay eggs of
similar mass (18 g), exhibit an RYD of 5–8 days
(Carey et al. 1980, Sotherland and Rahn 1987),
whereas Eurasian Kestrels (Falco tinnunculus)
have an RYD of only 9 days for eggs of 20 g
(Meijer et al. 1989). Shags (Phalacrocorax aristocelis), another altricial species, have an RYD of
13.5 days, similar to Barn Owls, for eggs weighing >40 g (Grau 1996). In Barn Owls, the yolk
mass/RYD duration ratio is only 0.3 in comparison to the average yolk mass/RYD ratio of 1.9
(0.1–9.0) for altricial birds with eggs of various
masses (1.6–330 g; calculated from values for 10
species from Carey et al. 1980, Walsberg 1983,
Sotherland and Rahn 1987, Astheimer and Grau
1990, Grau 1996). Barn Owls seem to have a
slower yolk-deposition rate than might be
expected considering its egg size. In addition,
the energy content of Barn Owl eggs is lower
than that for other altricial species (Durant et
al. 2000). As a consequence of those two factors,
107
Barn Owls have a lower daily nutritional
requirement per egg with two expected advantages. First, with a low daily deposition cost
per yolk, females can deposit simultaneously
relatively more yolk in follicles, within the
energy constraint of food intake. Interestingly,
laying order does not seem to have any effect on
the yolk growth rate in Barn Owls, indicating
that competition between follicles for nutrients
is small. The deposition of several eggs at the
same time is a phenomenon already described
for other birds (see below). Second, it could be
advantageous if food supply is limiting in terms
of energy or specific nutrients because the daily
requirement is smaller.
In Barn Owls, it was shown that the nutrients
required for egg formation could be obtained
by routine food intake in that species (Durant
et al. 2000). That relatively low daily nutritional
requirement is accentuated if we look at mass
relationship between egg and female (Walsberg
1983, Carey 1996). That relationship predicts
that Barn Owls should lay eggs weighing 25.5 g
instead of the 17.5 g found here (using the equation for cavity-nesting birds; log egg mass = log
0.61 + 0.631 log female body mass; Taylor 1994).
As a consequence, such small eggs may allow
Barn Owls to lay large clutches. However, laying small and numerous eggs could be a disadvantage if a longer posthatching development
period results in a higher predation rate for
nestlings (Halupka 1998). Barn Owls, like other
cavity-nesting species, are more secure from
predation (Martin and Li 1992).
O
F S
In our study, we showed that Barn Owls produced more follicles than eggs laid (Table 1) as
has been already observed in other bird species
(Haywood 1993). However, an original result is
that ovaries presented several atretic follicles at
the completion of the clutch. That indicated that
there was an ovum present ready to be ovulated
when the last egg was laid. Indeed, the removal
of eggs as soon as they are laid induces prolongation of laying, that is, egg development (stopped
aer the laying of 18 eggs; Y. Handrich pers.
obs.). Thus, surplus yolks may allow Barn Owls
to lay new eggs without an increase in the laying
interval. Barn Owl eggs hatch asynchronously
because of a start of incubation at the first laying. An increased laying interval would create
D
, M
, H
108
a large hatching interval for last-born chicks
with potential negative effects on their survival
(Durant and Handrich 1998, Durant 2002).
Barn Owls seem to be indeterminate layers
(Haywood 1993), birds that have great flexibility in the number of eggs they can lay. In
this species, the fact that the ovary produces on
average of 25 follicles during the laying period
certainly adds to that flexibility. In the field,
Barn Owls also show great plasticity in number
of eggs laid, with clutch sizes from 2 to 18 eggs
(Taylor 1994) in response to variations in prey
abundance (Mikkola 1983, Taylor 1994).
A
We thank C. Fritsch for help in laboratory analysis,
and G. H. Visser, J. Reynolds, T. J. Seller, D. A. Nelson,
K. G. Smith, and two anonymous referees for helpful
comments on an earlier dra of the manuscript. We
also thank J. Kent and D. Gremillet for editing help.
The experiments were done in compliance with current French laws and aer program acceptance by
French authorities: Authorisation of the Ministère de
l’Agriculture et de la Pêche n° 04196.
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Associate Editor: D. A. Nelson