J. Zool., Lond. (1998) 245, 137±145 # 1998 The Zoological Society of London Printed in the United Kingdom
Growth and food requirement ¯exibility in captive chicks of
the European barn owl (Tyto alba)
J. M. Durant and Y. Handrich
Centre d'Ecologie et Physiologie EnergeÂtiques, Centre National de la Recherche Scienti®que, F-67087 Strasbourg Cedex 02, France;
e-mail: handrich@c-strasbourg.fr
(Accepted 30 September 1997)
Abstract
The growth and the food requirements of the European barn owl (Tyto alba) were studied in three groups
of captive chicks. One group of chicks, raised in ad libitum food conditions by their parents, was used to
measure body mass and linear growth of a number of structural body components at their characteristic
growth rate. A second group of chicks, hand-raised with food ad libitum until ¯edging, was used to
measure food requirement at the characteristic growth rate. A third group, hand-raised with restricted
feeding, was used to specify the plasticity of growth and food requirements still compatible with a normal
development at ¯edging. Chicks of both sexes of the ®rst two groups experienced an overshoot in body
mass (maximum of 391 g) when approximately 40 days old, followed by a decrease (to a mass of 314 g)
until ¯edging at 60 days old, giving a mass distribution with age in the form of a bell-shaped curve. The
daily food intake also showed a bell-shaped curve with a peak value of 80 ‹ 10 g of fresh mice/day when the
body mass was maximum. The decrease of food intake preceding ¯edging was spontaneous. The average
daily food intake was 67 ‹ 17 g/day between the ages of 20 and 60 days. In the restricted feeding group,
however, the same timing for linear growth and ¯edging was achieved with a 17% reduction of daily food
intake. For the same ¯edging body mass as the ad libitum fed group, there was a ¯attening of the body
mass curve. The signi®cance of the overshoot in body mass and food intake is discussed in terms of the
chick's and brood's advantages and in terms of parental investment in this species with hatching
asynchrony.
Key words: Tyto alba, raptors, hatching asynchrony, brood requirement, logistic model
INTRODUCTION
In numerous bird species, the postnatal growth shows a
bell-shaped curve of body mass characterized by a peak
body mass heavier than that of an adult and a subsequent
decrease prior to ¯edging (review in Ricklefs, 1968). This
peak has been interpreted as a fat accumulation
(Lacombe, Bird & Hibbard, 1994) that must be reduced
prior to ¯edging by a reduction of food intake (Ricklefs,
1968; Ricklefs & Schew, 1994). The accumulation of
body reserves has been considered as an adaptation to
stochastic variation in foraging experienced by parents
(the energy insurance hypothesis). However, there is no
direct data to assert that the starvation period prior to
¯edging is not an endogenous phenomenon independent
of the chicks' food availability.
Hatching asynchrony, which is a breeding strategy
often observed in raptors, is generally interpreted as an
adaptation to stochastic variation in food availability
(brood reduction hypothesis; Lack, 1968). Different
species also show the characteristic bell-shaped growth
curve. In the American kestrel Falco sparverius
(Lacombe et al., 1994) it was demonstrated that a 10%
reduction of energy intake causes a disappearance of the
overshoot of body mass without any consequence for
body mass or body lengths at ¯edging time. In raptors
with a large clutch size (e.g. barn, snowy or short-eared
owl) and asynchronous hatching, we might expect the
effects of ¯uctuations in food availability to be intricate
since it could affect each chick according to birth rank.
In these situations, the possibility of modifying the
growth could be an advantage for chick survival and/or
for parental effort.
In the barn owl (Tyto alba), the ¯edglings (yearly
mean range 1.5±5.0; Taylor, 1994) leave the nest after
more than two months of growth. Interestingly, ¯edging
occurs about 20 days after attainment of peak body
mass (at 40 days of age: Pickwell, 1948; SchoÈnfeld &
Girbig, 1975; Baudvin, 1986; Wilson, Wilson & Durkin,
1987; Langford & Taylor, 1992; Taylor, 1994). Barn
138
J. M. Durant and Y. Handrich
owls are also known for yearly ¯uctuations of breeding
success (number of breeding pairs, second clutches,
clutch size) and nest mortality (Baudvin, 1978; Wilson,
Wilson & Durkin, 1986; Taylor, 1994).
We investigated the food requirements of captive
chicks during growth and the consequences of food
restriction on their growth parameters and growth
curve shape. Studies in captivity allow measuring
growth at its characteristic rate, which is possible only
when food availability is high (Ricklefs, 1973; Lenton,
1984). To understand the in¯uence of food intake on
chick growth, we compared groups of chicks raised
with food ad libitum with another group restricted in
feeding. The major objectives of this study were: (i) to
study the chick growth and the corresponding food
intake in situations of high food availability; (ii) to
learn if the decrease in body mass observed before
¯edging is spontaneous or results from a lessening of
food availability; and (iii) to determine the in¯uence of
restricted feeding on chick development and the impact
of this food restriction on the foraging investment of
the parents.
MATERIALS AND METHODS
This study was performed on 30 barn owl chicks from a
breeding programme conducted since 1985 in the
laboratory. The breeding programme was begun with 3
chicks born in captivity from road-injured birds kept in
a rescue centre. Whenever possible, new individuals of
the same origin were added. Each pair of owls was
housed in outside aviaries where a nest box was installed. The pairs bred at least once each year.
According to the type of rearing, we have constituted
3 groups of chicks as explained below.
Groups of birds
The growth of 50 chicks was followed for a ®rst group.
Subgroups were constituted after ¯edging, based on the
possibility of getting correct weighings (see below). We
selected 10 females out of 21 and 10 males among 29. In
this ®rst group (Control group, n = 20), chicks were
raised by their parents. The 10 males came from 5
different broods and 3 pairs of adults. The 10 females
came from 6 different broods and 4 pairs of adults.
Brooding occurred between March and July in outside
aviaries (5 6 4 6 2.5 m), the temperature ranging from
10±28 8C. Since the chicks were raised by their parents,
they were considered wild. This group was used as the
Control group. In ¯edging barn owls, sexing by external
features is not always reliable (Taylor, 1994; Handrich,
pers. obs.). Thus, when necessary, sexing was made by
laparoscopic examination of gonads under halothane
anaesthesia. The procedure complied with current laws
of French authorities: Authorization of the MinisteÁre de
l'Agriculture et de la ForeÃt followed by acceptance of
the research programme by the MinisteÁre de l'Environnement.
In the second group (Ad libitum group, n = 5), the
chicks (2 males and 3 females) came from 3 different
broods and 3 pairs of adults. Examination of the daily
food intake began when the chicks were 20 days old, the
age of thermal emancipation (Taylor, 1994). It was then
possible to house the chicks separately and alone in
open-topped nest boxes (25 6 25 6 50 cm) without the
need of female constant care. The boxes were put in a
climatic chamber that maintained the natural photoperiod (experiment conducted in June) and an ambient
temperature of 25 ‹ 1 8C. The thermal neutrality zone of
the barn owl is 22.5±33 8C (Johnson, 1974; Edwards,
1987).
In the third group (Restricted group, n = 5), the chicks
(3 males and 2 females) came from 3 different broods
and 3 pairs of adults. The chicks were raised under the
same conditions as the Ad libitum group except that
they were raised alone from their 12th day.
This corresponds to the time when the female starts
to forage during bad food years (Taylor, 1994). To limit
potential heat loss, cotton was added inside the nest
boxes.
Feeding
Chicks of the Control group were fed by their parents
with laboratory mice (Mus musculus). Daily, live mice
were put in the aviary at 16:00. At the same hour, we
checked food availability in the nest boxes so that we
could adjust the number of mice given.
Chicks of the Ad libitum group were also provided
with freshly killed mice at 16:00 each day. At 20 days
old, when the experiment started, they were able to eat
an entire mouse on their own (Taylor, 1994). Since mice
were always available when food was added, they were
considered fed ad libitum.
Chicks of the Restricted group were fed by hand with
pieces of fresh mice and thus the experiment could be
begun on 12-day-old chicks. In contrast with the Ad
libitum group, the meals were given 3 times daily
during daytime only (09:00, 12:30 and 16:00). The food
was ad libitum during meals only and not between.
During night-time (16:00±09:00), the chicks were given
no food. Since the meal-to-pellet interval for owls is
10±13 h (Duke, Evanson & Jegers, 1976), and is
certainly less for chicks fed with torn mice, the feeding
was not ad libitum but restricted. At the age of 20 days,
the chicks could feed by themselves and eat the food
stored inside the nest. Prior to 20 days old, the chicks
need to be fed by the female. As a consequence, chicks
younger than 20 days have no food available when the
female forages. They will be fed only when the female
stays in the nest to rest during daytime (Durant, pers.
obs.). This situation was simulated in the Restricted
group.
Growth and food intake in the European barn owl
Measurements
Body mass
The chicks were weighed to the nearest 0.1 g using a
Sartorius scale every day before the meal at 16:00 for
the Ad libitum group and the Restricted group but only
once every 2 days at the same hour for the Control
group. We veri®ed by checking the nest box before the
weighing that the last pellet was made. When no pellet
was found, the chick's belly was gently felt. This super®cial examination was done with great care and no
apparent consequences were observed for the birds.
Unreliable weighings (weighing with either pellet or
meal in stomach) were discarded.
Body size
Body length (humerus, tarso-metatarsus, tibia, rectrix
and remex) were measured with callipers to the nearest
mm on the Ad libitum and Control groups during the
afternoon weighing. Feather length corresponded to the
measurement of feathers plus the remnant of the sheath
which sticks out of the epidermis. Remex length was
taken to be the length of the tenth primary remex (P10).
Rectrix length was the length of the sixth rectrix from
the right (R1).
Growth curves and statistical analysis
To compare the growth data among groups and chicks,
we used the graphical method of Ricklefs (1967). A
logistic equation was ®tted to both body mass and
linear growth data for each individual (SigmaPlot 5.0
software from Jandel Scienti®c). Even if the logistic
equation does not describe a bell-shaped curve, we used
it for comparison purposes with other studies. Since the
body mass curve is bell-shaped, and because the logistic
equation describes a sigmoid curve, we divided the data
into 2 parts. The cut was made at the peak of body
mass, the 2 delimited parts approximating to a sigmoid
form well described by the logistic equation:
Y(t) = A [1+e-K (t ± ti)] -1
where Y(t) = body mass (g) or length (mm) of the chick
at age t (days), A = asymptotic body mass (g) or component length (mm), K = growth constant (1/day),
ti = in¯ection point of the growth curve (days).
The comparisons were made with the 3 parameters
obtained with the ®tting (A, K and ti) for each individual. The mean values of individual parameters and
their standard deviations were then calculated.
Statistical analyses were performed with non-parametric tests because of the small group sizes. The
Mann±Whitney U-test (MWU-test) was used for the
comparisons between sexes, the Kruskal±Wallis test to
compare the different groups and the Wilcoxon test to
compare changes in the same group.
139
Table 1. Differences between males and females in the Control
group. The ®tted parameters were obtained by the logistic
equation for each individual for different growth variables. A
is the asymptote (in g or mm), K is the growth constant (in
day-1) and ti the in¯ection point. The statistical analysis was
performed with the Mann±Whitney U-test using the individual
data. No statistical difference was found between sex for each
criterion (P>0.1). The values are means ‹ S.D.
Growth variables
Parameter
Body mass
A
K
ti
Humerus length
A
K
ti
Tarso-metatarsus
A
length
K
ti
Tibia length
A
K
ti
Rectrix length (R1) A
K
ti
Remex length (P10) A
K
ti
Males
(n = 10)
Females
(n = 10)
387.32 ‹ 15.04
0.175 ‹ 0.013
17.58 ‹ 1.11
92.48 ‹ 4.37
0.157 ‹ 0.048
13.13 ‹ 2.01
75.35 ‹ 4.17
0.150 ‹ 0.060
13.69 ‹ 2.25
97.54 ‹ 2.74
0.145 ‹ 0.031
12.04 ‹ 1.29
109.88 ‹ 2.10
0.135 ‹ 0.009
39.92 ‹ 1.59
203.27 ‹ 7.04
0.098 ‹ 0.003
40.50 ‹ 0.71
396.81 ‹ 19.86
0.180 ‹ 0.012
16.78 ‹ 1.51
92.85 ‹ 5.97
0.154 ‹ 0.039
13.45 ‹ 3.22
74.79 ‹ 6.68
0.140 ‹ 0.040
13.89 ‹ 2.85
97.75 ‹ 5.67
0.142 ‹ 0.030
12.11 ‹ 1.77
103.79 ‹ 11.10
0.142 ‹ 0.211
38.98 ‹ 2.23
200.55 ‹ 5.18
0.099 ‹ 0.004
38.98 ‹ 2.23
RESULTS
Growth in the Control group
Body mass differences between sexes
Although females tended to have an asymptotic body
mass greater than males (Table 1 and Fig. 1), the chicks
exhibited no signi®cant sex differences for the ®tted parameters (MWU-test, P>0.5). Data for males and females
were therefore pooled (Table 2 and curve in Fig. 1).
Body mass growth
The chicks were hatched with a body mass of 13.9 ‹1.4 g.
The gain of mass was almost linear between the 8th and
27th day (growth rate of 14.3 ‹ 1.3 g/day). Near the 40th
day, the body mass reached a maximum value of
391.0 ‹ 11.5 g (Table 2). Chicks grew from 10 to 90%
of their maximum weight in 25 days (the t10±90 index of
Ricklefs, 1968). Between the 40th day and ¯edging (60 to
65th day; Pickwell, 1948; Taylor, 1994), the birds lost
weight. Fledging body mass (314.4 ‹ 26.5 g) was signi®cantly less (Wilcoxon test, P<0.001) than the maximum
weight.
Linear growth
Bone and feather growth (Table 1) exhibited no
140
J. M. Durant and Y. Handrich
a
400
b
mass (g)
Body mass,
g
300
200
100
Males
Females
0
0
10
20
30
40
40
50
60
70
80
90
Age
Age,(days)
days
Fig. 1. Body mass (a) from hatching to maximum weight and (b) from maximum weight to 90 days of age (data for 10 males
and 10 females of the Control group and the logistic curve is for the sex-pooled data). The cross-hatched part of (b) represents
data already shown in (a).
Table 2. Fitted parameters obtained by the logistic equation for different growth variables in the Control group (n = 20). The
equation was ®tted to each individual chick. A is the asymptote, K the growth constant and ti the in¯ection point. The values are
means ‹ S.D.
Variable
Body mass
Humerus length
Tarso-metatarsus length
Tibia length
Rectrix length (R1)
Remex length (P10)
Parameter
A (g, mm)
K (day-1)
ti (days)
390.6 ‹ 11.5
91.59 ‹ 0.65
73.35 ‹ 0.61
96.57 ‹ 0.61
109.5 ‹ 0.60
201.9 ‹ 0.83
0.177 ‹ 0.003
0.150 ‹ 0.003
0.132 ‹ 0.004
0.140 ‹ 0.003
0.140 ‹ 0.003
0.099 ‹ 0.001
17.18 ‹ 1.35
12.41 ‹ 0.18
12.64 ‹ 0.22
11.37 ‹ 0.16
40.33 ‹ 0.17
40.37 ‹ 0.15
signi®cant difference in the ®tted parameters between
sexes (MWU-test, P>0.1 for the bones and P>0.1 for
the feathers). Therefore, data for males and females
were pooled (Table 2 and Fig. 2).
Humerus, tibia and tarso-metatarsus lengths were
12.0 ‹ 6.4, 15.2 ‹ 5.4 and 11.6 ‹ 4.4 mm, respectively, at
hatching. The three bones had nearly ®nished their
growth when the chicks were at their maximum weight
(98, 98 and 95% for humerus, tibia and tarso-metatarsus, respectively) and had reached full size at
¯edging. The remex (P10) began to grow out of the skin
near the 7th day and continued until the chicks left the
nest. At ¯edging, the remex had reached only 80% of the
asymptotic length. The rectrix (R1) began its growth
later than the remex at around the 17th day but grew
more quickly, with a length equal to 88% of the
asymptotic value at ¯edging. At the maximum of body
mass, the two types of feathers had reached only 47%
(P10) and 50% (R1) of their ®nal length.
Food intake and effect of diet on growth rate
There was also no signi®cant difference for the ®tted
parameters between the Control and Ad libitum groups
(MWU-test, P>0.1 in Table 3). We therefore considered
the Ad libitum group instead of the Control group, for
which we did not have the measurement of food intake,
as the reference for the relationship between food intake
and the characteristic growth.
The mean daily food intake was calculated over 4-day
intervals (Fig. 3a). In the Ad libitum group, daily food
intake increased, respectively, from the 20th to the 31st
day from hatching from 63 ‹ 5 to 80 ‹ 10 g/day. There
was then a spontaneous decrease to 60 ‹ 9 g/day around
the 60th day. The maximum and the minimum values of
food intake were signi®cantly different (Wilcoxon test,
P<0.001).
In the Restricted group, there was no signi®cant
change of daily food intake during the studied period of
Growth and food intake in the European barn owl
141
Table 3. Body mass ®tted parameters obtained by the logistic equation for groups reared in different conditions. The equation
was ®tted to each individual chick. Adult body mass is the body mass reached by the chicks of the experiment one year later. A is
the asymptote, K the growth constant and ti the in¯ection point. Values are means ‹ S.D. Values of the same column with
different labels are signi®cantly different (Kruskal±Wallis test, P<0.05; Dunn's test P<0.05)
Group
n
Control
Ad libitum
Restricted
Adult body mass (g)
20
5
5
100
a
317
337
317
Body mass
Maximum
390.6 ‹ 11.5
390.6 ‹ 35.0a
338.7 ‹ 8.26b
Fledging
92
Humerus
50
46
0
73
0
100
Tarso–metatarsus
50
36.5
0
97
0
100
Tibia
50
48.5
0
113
0
100
Rectrix
50
56.5
0
214
0
100
Remex
50
0
0
20
40
Age (days)
K (day-1)
A (g)
107
60
0
80
Fig. 2. Linear growth of various bones and feathers expressed
as a percentage of asymptote or in mm for the Control group
(logistic curves).
growth (maximum vs. minimum food intake, Wilcoxon
test, P = 0.09), despite a high value of 57 ‹ 15 g/day on
the 36th day. On a daily basis, the food intake of the
Restricted group was signi®cantly lower than in the Ad
libitum group (MWU-test, P<0.001). The food intake
during the studied period from age 20 to 60 days in the
Ad libitum group was on average 67 ‹ 17 g/day, i.e. 17%
higher than the Restricted group with a maximum difference of 28.5% at the Ad libitum peak of food intake.
The major in¯uence of the restricted diet on body
mass growth was the ¯attening of the bell-shaped curve
observed with the ad libitum diet (median asymptote
signi®cantly lower, Kruskal±Wallis test, P<0.003;
Dunn's test P<0.05; no signi®cant difference for the
growth parameters K and ti, Kruskal±Wallis test,
P = 0.051 and P = 0.651, respectively). Body mass at
¯edging time was calculated using the ®tted equation
for each chick. For the Restricted group, the value
was 298.9 ‹ 10.6 g and for the Ad libitum group
ti (days)
a
0.177 ‹ 0.003
0.174 ‹ 0.016a
0.215 ‹ 0.053a
17.18 ‹ 1.35a
17.67 ‹ 1.37a
16.26 ‹ 2.03a
317.7 ‹ 23.9 g. There was no difference in ¯edging body
mass or its timing (MWU-test, P>0.1 and Fig. 3b). The
body mass loss between the asymptote and the ¯edging
mass was 72.9 ‹ 17.8 g for the Ad libitum group which is
signi®cantly different from the 39.7 ‹ 13.3 g of the
Restricted group (MWU-test, P = 0.016). Feather
growth parameters showed no signi®cant difference
between the two groups (MWU-test; A, P = 0.305; K, P
= 0.176; and ti, P = 0.176).
DISCUSSION
Compared to previous data (Wilson, Wilson & Durkin,
1987; Langford & Taylor, 1992; Taylor, 1994), the new
information brought by the present study on barn owls
was the measurement of the chicks' food intake during
their growth. Our data enhance our knowledge on the
signi®cance of the bell-shaped curve encountered in
many species of birds (Ricklefs, 1968; Olendorff, 1974;
KorpimaÈki, 1981; Dijkstra, 1988; Lessells & Avery,
1989; Holt, Melvin & Steele, 1992; Hamer & Hill, 1993;
Lacombe et al., 1994; Starck, KoÈnig & Gwinner, 1995;
Kristan, GutieÂrrez & Franklin, 1996) by showing:
I. That the decrease in body mass that occurs before
¯edging is not due to a reduction of parental care but
results from a spontaneous reduction of food intake.
II. That a normal development occurs when the bellshaped growth curve, i.e. the overshoot, is ¯attened by a
reduction of food availability.
Characteristic growth rate of the barn owl
Field data are available on body mass and linear growth
for various subspecies of barn owls (Pickwell, 1948;
Ricklefs, 1968; SchoÈnfeld & Girbig, 1975; Lenton, 1984;
Wilson et al., 1987) and for the present subspecies, Tyto
a. alba (GueÂrin, 1928; Bunn, Warburton & Wilson,
1982; Baudvin, 1986; Langford & Taylor, 1992; Taylor,
1994). There is no difference between our data and
those found in other studies conducted on a larger
number of birds for the same subspecies (for parameters
calculated from GueÂrin's data 1928; for the asymptotic
body mass, Baudvin, 1986; Langford & Taylor, 1992;
Taylor, 1994; for the t10±90 index, De Jond in Wijnandts,
1984). Therefore, we may conclude that our Ad libitum
group exhibited the normal, characteristic, growth rate
(Ricklefs, 1973; Lenton, 1984).
142
J. M. Durant and Y. Handrich
Our growth constant (K, body mass) for the European barn owl was 0.177 which is low if we consider the
adult body size of the bird (Ricklefs, 1968). The European barn owl nests inside buildings which give a
protection against predators and climatic variations.
Furthermore, the female stays continuously with her
brood during the ®rst 20 days of development. Ricklefs
(1968) found that hole-nesting birds such as barn owls
usually have a lower growth rate than open-nesting
birds. This could explain the difference of growth rate
encountered with other owl species of similar size (Asio
otus, Wijnandts, 1984, or Asio ¯ammeus, Holt et al.,
1992). On the other hand, the characteristic growth rate
certainly has an endogenous origin. The barn owl is a
species originating from warm climates (Taylor, 1994).
This could explain its low growth rate and longer
breeding period in comparison with more northern
species such as the short-eared or the long-eared owl.
The Restricted group's diet simulates food intake of the
youngest chick of a wild brood
In barn owls, 20 days is a critical age in development.
Chicks become thermally emancipated (Taylor, 1994)
and begin to eat prey by themselves. Before 20 days, the
chicks need female care to be fed with torn prey. The
female starts to forage for long periods at night when
her youngest chick is between 12 and 20 days old (Bunn
et al., 1982; Taylor, 1994) and still unable to eat by
itself. Consequently, when the female is foraging, the
youngest chick may suffer food restriction because of its
incapacity to eat the food available in the nest. The
youngest chick can take its ®rst meal of the day only
when the female stays in the nest at the end of the night
to rest, a period when chicks seldom eat (Durant, pers.
obs.). The youngest chick will then eat only during
daytime (female resting period) like the chicks of our
Restricted group. Thus, our Restricted group reproduces the situation experienced by the youngest chick in
the wild. Since there was no apparent in¯uence of this
hypocaloric diet on the timing of development in this
experimental group, we may also assume that there is
none for the youngest ¯edgling of a wild brood in a year
of normal prey availability.
Food intake of captive birds is lower than in the ®eld
For chicks fed ad libitum, we calculated the average
daily food intake to be 67 ‹ 17 g/day (Fig. 3a). This
average value is overestimated because the calculation
was made from the age of 20 days to ¯edging, therefore
not taking into account the period of lesser food intake
the ®rst few days after hatching. From ®eld observations
(Durant, Gendner & Handrich, 1996), we estimate the
average number of prey brought to the nest per chick to
be 2.9/day. With an average prey's mass of 23.6 g
(Durant, pers. obs.), each chick could obtain 68.4 g a
day, which is nearly the same as the average daily food
intake we calculated. The main prey of the European
barn owl during the brooding period in eastern France
is the common vole Microtus arvalis (Muller, 1991).
Using the average caloric values for laboratory mice of
7.35 kJ/g (Handrich, Nicolas & Le Maho, 1993) and for
the common vole of 7.74 kJ/g (Wijnandts, 1984), we
could calculate energy intake. The gross energy intake
for wild chicks (529.4 kJ/day) was then 7.4% greater
than for captive chicks (493 kJ/day). This difference
might be due to an over-estimation of the number or
size of prey actually delivered to a chick in the ®eld.
Indeed, food storage is frequently observed in the nest
(Baudvin, 1980; Bunn et al., 1982; Taylor, 1994).
Another explanation could be a problem of dehydration for the wild chicks because the temperature in
certain nest sites (garrets, roofs or other protected
locations) can be more than 10 8C higher than the
outdoor ambient temperature (Durant, pers. obs.). Dehydration could increase the chicks' requirements,
especially if they consume stored, and thus also partially
dehydrated, prey. As a consequence, food ef®ciency
might be lower (rate of increase in body mass per unit
food intake; BjoÈrntorp & Yang, 1982; Brownell et al.,
1986) in the ®eld than in captivity.
Growth overshoot and spontaneous drop in food intake
Our results on barn owls in captivity support the idea
that the overshoot of body mass does not seem indispensable for the ¯edgling (for petrels, Ricklefs & Schew,
1994; for kestrels, Lacombe et al., 1994). Why then do
chicks undergo such a development? Lacombe et al.
(1994) demonstrated that, despite the same developmental timing, chicks fed ad libitum and having a peak
body mass were fatter than underfed chicks at ¯edging.
This observation is consistent with the energy insurance
hypothesis (Ricklefs & Schew, 1994), which predicts that
chicks accumulate fat as insurance against periods of
poor feeding conditions. On the other hand, Lacombe et
al. (1994) found a difference in fat reserves only for
chicks reared with at least a 30% food restriction. The
difference of overshoot between our two groups may
not be only the result of the accumulation of energy
reserves because we experimented with a food restriction
of only 17%. At the body mass peak, the feather growth
is at its maximum (ti in Table 2) and requires abundant
protein and water (Murphy & King, 1991; Dietz, Daan
& Masman, 1992). The reserves could be either proteins
or water but the water loss when feather synthesis ends
cannot explain the decrease in food intake we observed.
Nevertheless, it could be advantageous to constitute
reserves when possible instead of depending only on
food supply when the need is the most important. When
50% of the feather growth is completed (ti), the chicks
may start using the reserves to reduce the body mass for
the ¯edging. Since the feather development was normal
in the Restricted group, the energy, protein and water
inputs were suf®cient. Thus, the reserves may be more a
protection against a period of hypothetical food scarcity
Growth and food intake in the European barn owl
90
320
a
α
300
Brood food intake (g)
Food intake (g/day)
80
70
γ
60
β
γ
50
40
260
240
220
200
300
Body mass
300
200
200
Remex
100
10
20
30
40
Age (days)
50
60
100
Remex length (mm)
Body mass (g)
Restricted feeding
180
b
0
Ad libitum feeding
280
30
0
143
70
Fig. 3. Food intake and growth of the Ad libitum and Restricted groups. (a) Mean daily food intake based on a 4-day
interval in relation to age (open bars for the Ad libitum group
and cross-hatched bars for the Restricted group). The difference between extreme values (maximum and minimum) was
tested. Values with different labels are signi®cantly different
(P<0.05). The dashed curve corresponds to an extrapolation
of daily food intake before food measurements began when
the chicks were 20 days old. (b) Mean body mass and mean
remex length in relation to age (solid curve for the Ad libitum
group and dotted curve for the Restricted group). The open
circles correspond to the mean logistic body mass curves. The
signi®cantly different part is delimited by the two vertical
segments.
(Ricklefs & Schew, 1994) than an accumulation of
protein and/or water for the period of maximum growth
rate. In times of food scarcity, the barn owl changes its
diet (Taylor, 1994), which would change the intake of
essential amino acids, e.g. cysteine (Murphy & King,
1991) for feather synthesis. In such a case, the limitation
for feather growth would be the availability of the
essential amino acids (protein). It would then be advantageous for a chick to have stored essential amino acids.
Such a chick would experience normal growth at the
same time that a chick with no overshoot would experience growth delay. The composition of the energy,
water and protein reserves could be measured by body
composition throughout the growing period. Apparently such a study has never been done. The amount of
overshoot could also have an effect on the post-¯edging
survival, a period when the young are forced to hunt by
themselves. Since no difference was found for body
mass and size at ¯edging, the effect of the overshoot on
30
40
50
60
First hatched chick's age (days)
70
Fig. 4. Brood food requirement in relation to the age of the
®rst chick. Food requirement was calculated for a brood of
four chicks with a hatching asynchrony of 2.5 days for both
the Ad libitum group and the Restricted group.
subsequent survival could be due to only internal
factors. Consequences of the overshoot value can be
assessed only by body composition analysis.
The present work demonstrates that the body mass
decrease in ad libitum conditions, consecutive to the peak
of body mass, is the consequence of a spontaneous
decrease of food intake. What would be the advantage of
this kind of growth for parental investment ? We can
calculate the brood requirement for a hypothetical
brood fed ad libitum (Fig. 4; calculation made for a
brood of four chicks with a hatching asynchrony of 2.5
days). The two-day period of maximum brood requirement (Fig. 4) in ad libitum conditions is obviously an
important parameter of parental investment which
cannot be modi®ed. It depends only on the delay of the
hatching asynchrony (in a synchronized brood, the duration for the maximum requirements would be 16 days).
The short duration of the peak brood requirement is, in
addition to the hatching asynchrony, a consequence of
the spontaneous reduction of chick food intake when the
asymptotic body mass is reached (Fig. 3a, b).
For the brood, the energy that becomes available by
the spontaneous decrease of food intake of a given chick
could be transferred to its younger siblings at their
maximum food requirement period. Resources would
therefore not be wasted on the ®rst hatched chicks but
used to improve the growth of younger siblings. Moreover, the maximum food requirement is dispatched over
a longer period of time (Peak load hypothesis; Mock &
Schwagmeyer, 1990). As a consequence, brood reduction would not occur before a more severe food
restriction.
For the female, shortening the time of the peak brood
requirements allows the transfer of a part of the food
supply, i.e. the male investment, from the brood to the
restoration of her body reserves in preparation for an
eventual second brood. This would be an important
bene®t in a species like the barn owl where a second
144
J. M. Durant and Y. Handrich
brood could overlap with the end of the ®rst brood
(Muller, 1990). Thus, for the parents, an advantage of
the bell-shaped growth curve that gives a greater ¯exibility of chick requirements could be a decrease of the
in¯uence of food availability on parental investment.
If a comparison is made between the hypothetical
brood fed ad libitum and another one fed with the
restricted diet used in the present study (Fig. 4), we
would expect a 20% decrease of the peak food intake
(calculation made for a four-chick brood with a
hatching asynchrony of 2.5 days). The parents could
have raised at least one more chick with the restricted
diet, but the youngest chick would experience a growth
delay whenever there is a decrease of food supply
(Lacombe et al., 1994). Because of this growth delay,
even if the food shortage is of short duration, the
youngest chick could suffer from starvation when the
female is foraging. Moreover, the whole brood could
suffer a growth delay if the food restriction lasts longer.
Thus, this margin in food intake can be interpreted as a
safety asset against small ¯uctuations of food supply
without brood reduction.
CONCLUSION
The food intake of barn owls in captivity undergoes a
spontaneous decrease after the body mass has reached
its maximum value. This spontaneous reduction of food
requirement of the oldest chicks of a brood when the
youngest are at their peak requirement could be an
advantage for raising a brood successfully.
A reduction of food availability does not seem to
affect the development of barn owl chicks before ¯edging except for a reduction of the maximum body mass.
The body reserves that contribute to the overshoot of
body mass seem to be a security against periods of food
scarcity. As a consequence, a short period of food
restriction would have no effect on the development
(growth delay, brood reduction) since the reserves will
cover the needs (energy, water and protein).
Acknowledgements
We thank Erkki KorpimaÈki, Henk Visser, Denver W.
Holt, Yvon Le Maho, Charles A. Bost, Sylvie Massemin
and members of the laboratory for helpful comments on
various drafts of this paper. We also thank Christine
DualeÂ, Fleur Semensatis and Guillaume Froget for their
help with the English.
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