Prey selection and foraging performance of breeding Great Tits Parus major in relation to food availability

Abstract

Naef-Daenzer, L., Naef-Daenzer, B. and Nager, R. G. 2000. Prey selection and foraging performance of breeding Great Tits Parus major in relation to food availability. - J. Avian Biol. 31: 206-214. We studied the nestling diet and the foraging performance of Great Tits in relation to prey abundance in the field. Numerous experimental studies present data on foraging decisions in captive Great Tits. Little is, however, known about prey selection in the field in relation to the food available and the consequences this has for the food delivery rate to nestlings. Since the foraging performance of the parents is one of the main determinants of fledging weight and juvenile survival, foraging behaviour is an important part of Great Tit reproduction. During the early breeding season up to 75% of the prey biomass delivered to the nestlings were spiders, which is in contrast with other studies. Only when caterpillars reached a size of 10-12 mg (approximately the average size of the spiders caught at that time) did the Great Tits change their preferences and 80-90% of the delivered prey masses were caterpillars, as reported by other authors. This 'switching' between prey occurred within a few days. It was not related to the changes in abundance but to size of caterpillars. The rate at which caterpillars were delivered to the nestlings (in mg:nestling:h) was strongly correlated with the caterpillar biomass available (in mg:m of branches) and nestling growth rate was significantly influenced by the mass of available caterpillars. The results provide evidence why perfect timing of breeding is so important for the Great Tit, and contribute to the understanding of the causal link between food supply, growth and breeding success.

Full text

JOURNAL OF AVIAN BIOLOGY 31: 206–214. Copenhagen 2000
Prey selection and foraging performance of breeding Great Tits
Parus major in relation to food availability
Luzia Naef-Daenzer, Beat Naef-Daenzer and Ruedi G. Nager
Naef-Daenzer, L., Naef-Daenzer, B. and Nager, R. G. 2000. Prey selection and
foraging performance of breeding Great Tits Parus major in relation to food
availability. – J. Avian Biol. 31: 206 – 214.
We studied the nestling diet and the foraging performance of Great Tits in relation
to prey abundance in the field. Numerous experimental studies present data on
foraging decisions in captive Great Tits. Little is, however, known about prey
selection in the field in relation to the food available and the consequences this has
for the food delivery rate to nestlings. Since the foraging performance of the parents
is one of the main determinants of fledging weight and juvenile survival, foraging
behaviour is an important part of Great Tit reproduction. During the early breeding
season up to 75% of the prey biomass delivered to the nestlings were spiders, which
is in contrast with other studies. Only when caterpillars reached a size of 10–12 mg
(approximately the average size of the spiders caught at that time) did the Great Tits
change their preferences and 80–90% of the delivered prey masses were caterpillars,
as reported by other authors. This ‘switching’ between prey occurred within a few
days. It was not related to the changes in abundance but to size of caterpillars. The
rate at which caterpillars were delivered to the nestlings (in mg/nestling/h) was
strongly correlated with the caterpillar biomass available (in mg/m of branches) and
nestling growth rate was significantly influenced by the mass of available caterpillars.
The results provide evidence why perfect timing of breeding is so important for the
Great Tit, and contribute to the understanding of the causal link between food
supply, growth and breeding success.
L.Naef-Daenzer,B.Naef -Daenzer,Swiss Ornithological Institute,CH -
6204
Sempach,
Switzerland.E-mail
:
beat.naef@6ogelwarte.ch.R.G.Nager,Ornithology Group,Gra-
ham Kerr Building,Institute of Biomedical and Life Sciences,Uni6ersity of Glasgow,
Glasgow G
12 8
QQ,Scotland,UK.
The timing of the breeding season of birds is ultimately
adjusted to the availability of their food (Lack 1968).
Among the best studied systems are tits (Parus spp.) of
temperate deciduous forests. Their main prey during
breeding is various species of caterpillars living in tree
foliage. It is now commonly observed that birds raising
their young at times with highest caterpillar abundance
have the highest reproductive output (e.g. Tinbergen
and Boerlijst 1990, Nager and van Noordwijk 1995, van
Noordwijk et al. 1995, Dias and Blondel 1996). To
understand the seasonal pattern in reproductive success
we need to understand the proximate mechanisms that
link foraging decisions and fitness. Higher food
availability results in better growth (Keller and van
Noordwijk 1994), and better growth improves survival
and recruitment chances of the offspring (Tinbergen
and Boerlijst 1990, Gebhardt and van Noordwijk 1991,
Verboven and Visser 1998). However, the underlying
mechanism of this relationship between food availabil-
ity and breeding success for Great Tits Parus major
remains largely unexplored.
How prey selection and searching behaviour are af-
fected by the availability and quality of prey has been
discussed extensively at the theoretical level (Charnov
1976, Lessells and Stephens 1983, Stephens and Krebs
1986). Although there are excellent studies on foraging
decisions in captive Great Tits (e.g. Smith and Sweat-
man 1974, Krebs et al. 1977, 1978, Ydenberg 1984)
little is known about foraging decisions in relation to
food availability in natural conditions. To discuss prey
selection in relation to abundance an assessment of
both variables is necessary. Earlier studies have de-
© JOURNAL OF AVIAN BIOLOGY
JOURNAL OF AVIAN BIOLOGY 31:2 (2000)
206

scribed the nestling diet of Great Tits, but the seasonal
development of prey species available has not been
investigated with high temporal resolution (Tinbergen
1960, Gibb and Betts 1963, Royama 1970, van Balen
1973). Several more recent field studies on various bird
species analyse the foraging decisions in relation to prey
abundance in general (Great Tits, e.g. Barba and Gil-
Delgado 1990, Przbylo 1995, Riddington and Gosler
1995, Massa and Lo Valvo 1996; other bird species, e.g.
Krebs and Avery 1985, Brodmann 1994, Frey-Roos et
al. 1995, Illera and Atienza 1995). Detailed field studies
on prey selection including an assessment of prey
availability concerned other passerines and non-passer-
ines (Davies 1977, Goss-Custard 1977b, Turner 1982,
Thompson 1984). Here we present a study on the
nestling diet of Great Tits in relation to the seasonal
variation in prey availability, and its effect on the rate
at which energy is delivered to the brood. The investi-
gation considers two levels of analysis: (1) prey selec-
tion in relation to size and density of prey species and
(2) the foraging performance of tit parents in relation to
prey biomass available.
Methods
Data were collected from 27 April to 19 May 1990,
which is the main breeding season in the area, in a
mixed deciduous forest of 80 ha near Basel, Switzer-
land, 270 m a.s.l. Thirty percent of the forest canopy
trees are oaks (Quercus petraea,Q.robur). The remain-
der of the canopy includes ash Fraxinus excelsior (36%),
beech Fagus sil6atica (18%), and hornbeam Carpinus
betulus (10%). Since 1986 about 300 nestboxes had been
present in the forest.
Ten boxes were equipped with a photo-recorder con-
sisting of a Super 8 mm movie camera, a photocell
recording each passage of a bird, and an infrared
flashlight. Approximately 90% of all passages were
recorded. Failures occurred when the departure instead
of the entrance of a bird was recorded or when the flash
was insufficiently charged. A watch mounted inside the
nestbox gave the exact time when the pictures were
taken. The cameras were kept for 1 to 3 days at a given
box. To allow the birds to recover from the disturbance
and resume their normal feeding rate, records from the
first hour after camera installation and after daily in-
spection of the nestboxes were omitted. To avoid ad-
verse effects or premature fledging, observations were
restricted to broods where nestlings were 7–12 days
old. The brood sizes were 3, 4, 5, 6, 8 (one brood each)
and 7 (5 broods), respectively; the mean brood size was
6.1.
To analyse the effects of foraging conditions on
nestling growth, we used the method of growth analysis
developed by Keller and van Noordwijk (1993, 1994).
This method quantifies growth rates as a ratio of the
observed daily growth compared to the expected
growth under good conditions. Details of the technique
are given in Keller and van Noordwijk (1993). Here, we
give only a brief summary. Expected growth is evalu-
ated on the basis of a Richards growth function in
which the winter weights of parents were used as an
estimate of the asymptote of individual growth curves.
The ratio of the realised over the expected growth R is
independent of age and actual size and is used as an
estimator of the foraging conditions. R equals 1 if a
nestling grows as expected under good conditions.
We examined the photographs under a binocular
microscope (10–25 ×), determined the feeding time
and identified the prey species. We categorised the prey
as caterpillars (mainly Tortricidae, but also Geometri-
dae and Noctuidae), spiders, beetles (order Coleoptera),
and ‘other winged insects’, and ‘unidentified prey’. A
large proportion of unidentified prey consisted mainly
of a whitish mass similar to butter, probably some
fungus. The body length of caterpillars and spiders was
estimated by comparing it to the visible part of the
Great Tits bill, which had an average estimated length
of approximately 8 mm. Five size categories (multiples
of bill length) were discerned (58mm,9mm–16mm,
17 mm–24 mm, 25 mm – 32 mm, ]32 mm). The mass
of caterpillars was estimated from an empirical calibra-
tion curve derived from caterpillars collected from 401
branch samples, as described below. The mass of spi-
ders was calculated using the equation y=0.35x
2.36
,
where y is the mass in mg and x is body length in mm
(Lille 1996). As caterpillars and spiders this time of the
year contain a similar amount of water (around 74%
and 69%, respectively, Brodmann 1994), we refer to
fresh weights. As ‘winged insects’ were not identified to
the level of species, this category comprises animals of
quite different shapes, and no estimate of size was
attempted.
We used a skylift reaching 35 m in height to assess
prey composition and density in the canopy of trees,
which is the main foraging habitat during breeding
(Glutz von Blotzheim and Bauer 1993). Two to six
samples were taken weekly from 30 trees for six weeks.
The branches were removed after enclosing them in a
800 l plastic bag. Samples were stored at field tempera-
tures and examined within four days of collection.
Samples that were examined later than four days after
collection were excluded from the analysis. Caterpillars
and other invertebrates were counted and stored in
alcohol. The lengths of the twigs with a diameter of less
than 1 cm (i.e. the parts carrying leaves), were measured.
For 401 branch samples, the mass and length of all
caterpillars were determined to the nearest mg and mm,
respectively. From these data a calibration curve relat-
ing these two measures was determined (Fig. 1). Dates
are given here as continuous numbers with 1 March=
1. The mean caterpillar hatching date in 1990 was 21
207
JOURNAL OF AVIAN BIOLOGY 31:2 (2000)

Fig. 1. Relationship between length (mm) and mass (mg, fresh
weight) of caterpillars on the four tree species (y=0.08x
2.21
,
r=0.95, n=1412). The data stem from 401 branch samples
collected at the study site during the study.
Fig. 2. Density (number of prey per m branch) of four prey
types on trees and their proportion in the nestlings’ diet during
the course of the breeding season. Each triangle is the average
for one nest. The averages per day and nest (dots) are also
shown. The density scale is given on the right y-axis, the
proportion scale on the left y-axis. Note the scale differences
between the prey species on the y-axes.
March. All statistical analyses are based on averages
per box. The figures also show the daily averages.
Results
Nestling diet
The Great Tit is usually a single-prey loader; 6.4%9
10.7 (median9s.e.) of all prey were brought in double-
prey loads. Caterpillars and spiders were the major
components of the nestling diet, winged insects con-
tributed up to 20% and beetles rarely more than 2% by
prey number (Fig. 2). Unidentified prey were more
important before day 68, when they accounted for up
to 20% of prey items; on average 8.9%98.9% (s.e.) of
all prey remained unidentified. From the end of April
to mid May considerable changes in the composition of
the nestling diet were observed. Birds nesting early fed
their young mainly spiders (Fig. 2); by day 60 (end of
April), 60–70% by number of diet items fed to the
nestlings were spiders but by day 63 spiders only ac-
counted for 10% of the nestling diet. Simultaneously
the proportion of caterpillars in the nestling diet in-
creased from 20% to 60–80%, and for the rest of the
observation period caterpillars dominated the nestling
food. Winged insects were brought in variable propor-
tions. Beetles constituted up to 4% of the early nestling
diet but after day 63 dropped to almost zero.
If we consider prey numbers, the pattern observed in
the nestling diet mostly did not reflect the abundance of
the prey types in the environment. Whereas the propor-
tion of caterpillars in the nestling diet increased, the
caterpillar density in the trees declined over the same
period (Fig. 2). Similarly, whereas the density of spiders
in the trees showed a threefold increase over the obser-
vation period, their proportion in the nestling diet
decreased dramatically.
JOURNAL OF AVIAN BIOLOGY 31:2 (2000)208

Winged insects were taken in proportions which did
not reflect their density on trees either. The very small
proportion of beetles in the diet was not related to
their density on trees. Only before day 65 were they
collected to any extent.
As a measure of the preference of Great Tits for a
particular prey type we used its relative frequency in
the diet (number of prey x taken/total number of prey
taken) compared to its relative frequency on trees
(number of prey x available on trees/total number of
potential prey available on trees). Early in the season
caterpillars were caught less frequently than expected
from their abundance on trees (Fig. 3); the tits’ prefer-
ence increased continuously, until after day 63 they
were caught approximately according to their relative
frequency on trees, and after day 73 they were strongly
preferred. In contrast, spiders were strongly preferred
during the early season; this preference decreased con-
tinuously until day 73 from which date on they were
caught according to their relative frequency on the
trees. Winged insects were always taken much below
their relative frequency on trees.
Prey size selection
Early in the season Great Tits selected caterpillars well
above the mean caterpillar size available; the mass of
the average caterpillar delivered to a brood was 2.6
times the mass of caterpillars on trees (Fig. 4). For
example, on day 65 the mean weight of the caterpillars
on trees was 18 mg, whereas the tits fed their young
with caterpillars of an average weight of 46 mg. The
mean size of caterpillars available peaked at day 73
and then decreased due to the hatching of other cater-
pillar species. From day 67 to 80 the selected caterpil-
lars were still heavier than the average caterpillar on
trees, but the selection for the biggest items was less
marked than earlier in the season.
Great Tits switched from spiders as their main prey
type to caterpillars when, around day 62, the mean
weight of caterpillars on trees reached c. 15 mg (Fig.
5) and the caterpillars selected for the nestlings
weighed around 40 mg (Fig. 6); the caterpillars now
amounted to 60–80% (by number) of the diet. Al-
though spiders contributed less than 10% of the diet
for the rest of the observation period, they were, in
relation to their density, still very much preferred (Fig.
3). Overall the mean weight of caterpillars was greater
than the mean weight of spiders (Fig. 6; ANCOVA,
corrected for date, df=1; 17, F=10.15, p B0.005).
The preference for a prey type and the switching were
not related to the age of the nestlings within the age
span studied (7–12 days), but to the date, which repre-
sents the development of the prey species on the trees
(Fig. 7). Early in the season the nestling diet contained
a high percentage of spiders for all nestling ages, and
later the percentage was low even for nestlings aged 7
days.
Foraging performance
The amount (mg) of caterpillars the Great Tit parents
delivered per hour and per nestling was correlated with
Fig. 3. Proportions of three different prey species in the diet of
the nestlings in relation to their proportions on trees. Triangles
represent averages per nest, dots averages per day and nest.
Note the linear scale on the y-axis for ‘winged insects’. A value
above 1 means that the prey species was taken more often than
expected from its relative frequency on trees.
209JOURNAL OF AVIAN BIOLOGY 31:2 (2000)

Fig. 4. Mean weight (mg) of caterpillars on trees (solid line),
75% percentile (dashed line) and maximum weight of caterpil-
lars on trees (dotted line), respectively, and weight of caterpil-
lars brought to the nest. Triangles represent averages per nest,
dots averages per day and nest. The average mass of caterpil-
lars on trees increased until about day 74. Then the earliest
species pupated and small new caterpillars appeared, so that
the average caterpillar mass diminished.
Fig. 6. Seasonal development of the mass of caterpillars and
spiders brought to the nest. The values for caterpillars are
represented by triangles (y=10.99+0.45x, r=0.46); the val-
ues for spiders are represented by dots (y=11.61=0.31x,
r=0.34). Big symbols represent averages per box, small sym-
bols averages per day and box. The masses of caterpillars and
spiders differ significantly (ANCOVA, df=1; 17, F=10.15,
pB0.005).
the development of the caterpillar biomass (mg/m) on
the trees (Fig. 8; y=−208.76 +195.93 · log x, r =0.88,
pB0.001).
The mass of caterpillars delivered per hour (mg cater-
pillars/hour) was influenced by caterpillar biomass and
brood size (Table 1). These two variables explain 83%
of the variance. Thus the rate at which Great Tits
delivered prey to the brood was influenced by both the
abundance of their main food at the time and the
number of young they had to feed.
We found a strong relationship between the average
nestling growth rate R per brood and the size (mg) of
available caterpillars (Fig. 9; y
0.5
=1.28−8.05/x, n=
10, r=0.92, pB0.0001). This result indicates that the
availability of large prey has an immediate effect on the
growth performance of tit nestlings. Furthermore, it
confirms radiotracking data (Naef-Daenzer and Keller
1999) showing that the average search time per feeding
is a function of both caterpillar size and density.
Feeding frequency
As the mass of prey items varied considerably, feeding
frequency does not provide accurate information about
the amount of food delivered to the young. The feeding
frequency per hour was negatively influenced by date
and positively by brood size (Table 2). The two vari-
ables explain 81% of the variance. Tits with larger
broods and tits breeding early, when caterpillars were
small and nestlings were mainly fed spiders, had to
bring food more often. The feeding frequencies are
Fig. 5. Relationship between the proportions of caterpillars
and spiders in the nestling diet in relation to the average
weight of caterpillars on trees. Values for caterpillars are
represented by triangles, values for spiders by dots. Big sym-
bols represent averages per box, small symbols averages per
day and box.
JOURNAL OF AVIAN BIOLOGY 31:2 (2000)210

Fig. 7. Percent of spiders (in
numbers) in the diet in relation to
date and nestling age. The averages
per day and nest are shown. The
amount of spiders in the diet is not
dependent on nestling age.
Fig. 8. The mass of caterpillars the parents brought per
nestling and hour as a function of caterpillar biomass on trees.
Big symbols represent averages per box, small symbols aver-
ages per day and box. y=−208.76 +195.93 · log x, r=0.88,
pB0.001.
comparable to those observed at the same time for
radio-tagged birds (Naef-Daenzer and Keller 1999).
By increasing the feeding frequency parents with
larger broods were able to maintain an almost constant
level of food provisioning per nestling (Fig. 10). The
above result showing that the brood size positively
influences the amount (mg) of caterpillars delivered per
hour points in the same direction. Fig. 10 shows also
how, in an early brood, caterpillars were substituted by
an almost equal amount of spiders.
Discussion
Numerous field studies describe the nestling diet of
Great Tits in various habitats (e.g. Betts 1955, Gibb
and Betts 1963, van Balen 1973, Cowie and Hinsley
1988, Barba and Gil-Delgado 1990). In contrast to
them we additionally investigated prey abundance in
detail. This enabled us to relate foraging decisions and
performance to food availability. The application of
foraging theory to wild animals has been criticised
because it introduces simplifications and avoids con-
straints in models of animals’ foraging behaviour (Lu-
cas 1987, Grundel 1990). The assumptions of foraging
theory are often not met in the field situation. For
example, only some prey species are evenly distributed,
211
JOURNAL OF AVIAN BIOLOGY 31:2 (2000)

while others show a clumped distribution, as our
branch samples revealed. But the main drawback of the
assumptions is that, unlike in the laboratory, prey
species in the wild grow and they move between
patches. Thus prey encounter rates keep changing in
time and space. Therefore, in order to forage optimally
an animal needs to collect information about food
availability. Many models, however, assume a forager
either to have such information or to forage at random.
Observations of radio-tagged Great Tits provide evi-
dence that the birds return several times in sequence to
profitable patches, but keep exploring other sites con-
tinuously (Naef-Daenzer and Keller 1999).
Although many possible factors were not controlled
for in this field study, some rules proposed by foraging
theory were confirmed: the tits preferred larger prey to
smaller and much more frequent prey. At the beginning
of observations spiders were bigger and preferred to the
caterpillars, which were much more numerous but
small. Although spiders contributed little to the diet
later in the season, in relation to their relative density
they were preferably collected throughout the study.
Royama (1970) proposed for Parus major minor in
Japan that young nestlings might need spiders because
these contain some nutrient important for their devel-
opment. He observed the highest spider proportion in
the diet of nestlings of ages 5–6 days. However,
Royama presented no data on the seasonal abundance
of prey species. Our results indicate for the ages 7–12
days that the changes in the diet were entirely related to
the seasonal development of prey biomass. Grundel and
Dahlsten (1991) confirmed Royama’s observations for
Mountain Chickadees Parus gambeli. In contrast to
this, Betts’ observations (1955) of the diet of one brood
of Great Tits look similar to our data for the age 7 days
onwards. Other authors have shown for other bird
species that food items are not only selected to max-
imise the amount of food brought to nestlings but also
its quality (Goss-Custard 1977a, Krebs and Avery
1985). In contrast, Brodmann (1994) found in his de-
tailed study of Water Pipits Anthus spinoletta that food
quantity was more important than quality: the pre-
ferred prey species did not differ in regard to lipid,
carbohydrate, water or energy content compared to
other possible prey species present. The number of
fledglings was correlated with the amount of food
available, but not with the quality of prey. We show
Fig. 9. Relationship between caterpillar mass (mg) and mean
nestling growth rate R per nest. y
0.5
=1.28−8.05/x, r=0.92,
pB0.0001.
that by using the more profitable spiders early in the
season the tits could – in spite of the low caterpillar
weights – maintain an almost equally high rate of food
delivery (mg prey per hour and nestling) as could
parents taking caterpillars later in the season.
Throughout the observations the tits selected cater-
pillars which were by far heavier than the average
caterpillars on trees. Many authors have described this
selection for large size of prey in the nestling diet (e.g.
Tinbergen 1960, Gibb and Betts 1963, Davies 1977,
Brodmann 1994). A field study with radio-tagged tits
indicated that big caterpillars were found faster than
smaller ones (Naef-Daenzer and Keller 1999). The re-
duced searching time and the higher energy gain per
feeding trip make large caterpillars more profitable.
The tits’ diet was not influenced by the abundance of
winged insects, which had comparable densities to
caterpillars and were an order of magnitude more fre-
quent than spiders and beetles. Nevertheless winged
insects were caught in remarkably lower proportions
than caterpillars, and their proportion in the diet was
much below the frequency expected from their relative
density on trees. One reason might be that this group
Table 1. Multiple regression of caterpillar mass (mg) deliv-
ered per hour (dependent variable) in relation number of
nestlings and caterpillar biomass on trees. R
2
(adj)=0.86,
n=10 broods.
Coefficient SE p
Constant −705.91 219.47 0.015
Brood size 168.60 31.82 0.001
1.818.22 0.003Caterpillar biomass
Table 2. Multiple regression of nestling feeding frequency per
hour (dependent variable) and date, brood size and caterpillar
size on trees. R
2
(adj.)=0.81, n=10 broods.
Coefficient SE p
Constant 77.83 17.31 0.004
Brood size 4.84 1.22 0.007
0.002Date −1.44 0.27
0.17Caterpillar size 1.38 0.89
JOURNAL OF AVIAN BIOLOGY 31:2 (2000)212

Fig. 10. Relationship between brood size and mg caterpillars
per hour and nestling, and mg spiders per hour and nestling
delivered by the parents. The values for caterpillars are repre-
sented by triangles, values for spiders by dots. Big symbols
represent averages per box, small symbols averages per day
and box. The very low caterpillar delivery rates for the nest
with 5 young were observed at the beginning of the observa-
tion period, when spiders were the main part of the diet.
post-fledging survival (Tinbergen and Boerlijst 1990,
Gebhardt and van Noordwijk 1991, Verboven and
Visser 1998, Naef-Daenzer and Keller 1999). Although
there were indications that tits compensate for in-
creased demands of the brood, the energy flow to the
nest was mainly determined by the availability of prey
and much less so by the behaviour of the parents. Early
in the season the Great Tits substituted the small
caterpillars by an almost equal amount of spiders, but
the growth rate of their young was lower than during
the caterpillar peak. This makes clear that the parents’
performance is limited by the availability of profitable
prey, in this case, big caterpillars. The timing of the
brood with the time of maximum size and abundance
of caterpillars is therefore of greatest importance.
Acknowledgements – We would like to thank S. Gebhardt-
Henrich for her assistance in the field work. A. van Noordwijk
kindly offered the data for analysis. L. Keller provided growth
data for the observed broods. V. Keller and N. Zbinden gave
helpful comments on the manuscript. Financial support from
the Swiss National Science Foundation (grant number 3.153-
1.88) is gratefully acknowledged.
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(Recei6ed
12
January
1998
,re6ised
20
No6ember
1998
,accepted
19
March
1999
.)
JOURNAL OF AVIAN BIOLOGY 31:2 (2000)214