Behavioral Ecology
doi:10.1093/beheco/arr063
Original Article
Postfledging family space use in great tits
in relation to environmental and parental
characteristics
Thijs van Overveld, Frank Adriaensen, and Erik Matthysen
Evolutionary Ecology Group, Department of Biology, University of Antwerp, B-2020 Antwerp, Belgium
Parental care has been widely studied in birds and mammals, but variation in space use in family groups has received less attention,
despite its potential importance for both survival and subsequent dispersal of offspring. In this study, we evaluate factors affecting
postfledging family space use in a small territorial songbird, the great tit (Parus major). Family space use was monitored using radio
tracking. Our main objectives were 1) to quantify in detail the temporal and spatial scale of family movements, 2) to test behavioral
hypotheses explaining when and how frequently families leave their breeding territory, and 3) to test to what extent movements
were based on familiarity with the environment. We found that variation in space use was to a large extent due to some families,
but not others, regularly undertaking foraging excursions of up to more than a kilometer away. Daily excursion probability was
higher for families occupying low-quality territories, and consequently, these families covered larger areas during foraging.
Excursion behavior and range use also strongly depended on maternal breeding experience and personality. We further present
some striking examples of inexperienced mothers moving toward previously visited areas, suggesting that familiarity with the
environment plays an important role in patterns of space use. Overall, our results suggest that variation in family movements
reflects different foraging strategies in relation to parental characteristics. Key words: breeding experience, foraging strategies,
Parus major, personality, postfledging care, space use. [Behav Ecol 22:899–907 (2011)]
INTRODUCTION
any vertebrate species, in particular birds and mammals,
have extended periods of parental care during which
offspring are provided with resources and protected from
predators. This period of care often extends beyond the altricial stage when parents and offspring move in family groups
(Clutton-Brock 1991). This extended care not only allows offspring to be provisioned and protected but also to acquire
foraging and antipredator skills and more generally to acquire
information about their environment (Beecher and Burt
2004; Davis and Stamps 2004; Galef and Laland 2005;
Slagsvold and Wiebe 2007). In atricial birds, the period of
prolonged care, that is, from fledging till family break up,
most commonly referred to as the postfledging period, is considered a most important phase for parent and offspring
fitness because of high mortality rates (Naef-Daenzer et al.
2001; Sunde 2005; Yackel et al. 2006). Yet, information on
parental decision making and the ecological factors operating
during this phase still remain scarce with most studies so far
focusing on the duration of care provided (Verhulst and Hut
1996; Minguez et al. 2001; Gruebler 2007; Tarwater and Brawn
2010; Vergara et al. 2010). Much less is known, however, about
the movements parents may undertake with their depended
offspring, which often extend far beyond the pair’s breeding
territory and may vary greatly among different family groups
within the same species. These movements have been described for groups as diverse as songbirds (e.g., Drent 1984;
M
Address correspondence to T. van Overveld. E-mail: Thijs.vanoverveld
@ua.ac.be.
Received 29 July 2010; revised 15 January 2011; accepted 17
March 2011.
The Author 2011. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
Rivera et al. 2000; Adams et al. 2001; Cohen and Lindell 2004;
Berkeley et al. 2007; White and Faaborg 2008), raptors (e.g.,
Kennedy and Ward 2003; Mannan et al. 2004), owls (e.g., Delgado et al. 2009), parrots (e.g., Myers and Vaughan 2004), and
geese (e.g., Mainguy et al. 2006; Nack and Andersen 2006).
Recent work has shown that these family movements in territorial songbirds may have an effect on offspring dispersal (Matthysen et al. 2010) and patterns of mate choice (van de
Casteele and Matthysen 2006), but the behavioral mechanisms
underlying variation in postfledging family movements and the
link with juvenile dispersal still remain largely unexplored.
Movements as strategies of postfledging care may reflect
adaptive responses to changes in environmental conditions
such as the availability of food in the breeding territory, predation pressure, or time available for reproduction (CluttonBrock 1991; Stearns 1992). Postfledging movement strategies,
however, may be more complex with variation in space use differing among families depending on the way parents cope with
such environmental variation. For example, differences among
parents in breeding experience and/or familiarity with the local environment are likely to influence patterns of space use,
especially in the period after fledging, in which offspring food
demands may even be higher than during the nestling phase
(Poulsen 1996). Furthermore, familiarity with the local environment may be of particular importance in explaining family
movements in animals such as birds because of their small
and seasonal breeding territories. In most bird species, the territorial system breaks up when broods fledge, allowing much
greater flexibility in adopting different movement strategies
compared with year-round territorial species and/or species
with lower mobility, which may be largely restricted to forage
within well-established territorial boundaries.
Parents may also vary in ways of coping with environmental
condition depending on individual differences in personality
Behavioral Ecology
900
(Gosling 2001) or temperament (Reale et al. 2007). Different
personality types differ consistently in exploration (Verbeek
et al. 1994), information gathering (Benus et al. 1990), or
willingness to take risk (van Oers et al. 2004; Hollander
et al. 2008), and these aspects have recently been shown to
be associated with differences in space use (Boon et al. 2008;
Boyer et al. 2010; van Overveld and Matthysen 2010) and reproductive strategies (Both et al. 2005). Furthermore, the link
between personality and space use has also received considerable interest in the context of dispersal as, for example, in
great tits, where offspring from fast-exploring parents have
larger natal dispersal distances (Dingemanse et al. 2003).
Such a pattern may result from heritable variation in personality which in turn influences dispersal, but parents may also
influence dispersal directly via postfledging family movements
(Dingemanse et al. 2003; Matthysen et al. 2010).
In this study, we evaluate factors affecting postfledging
family movements in a small territorial songbird, the great
tit (Parus major). In this species, parents with dependent offspring frequently leave their breeding territories and escort
them to feeding areas over distances that widely surpass the
average territory size (Drent 1984; Matthysen et al. 2010). Our
main objectives were 1) to quantify in detail the temporal and
spatial scale of family movements, 2) to test behavioral
hypotheses explaining when and how frequently families leave
their breeding territory, and 3) to test to what extent movements were based on familiarity with the environment.
We tested 3 main hypotheses concerning the behavioral
mechanism explaining movement behavior. First, we tested
whether movement behavior of families varied in response
to environmental factors such as territory quality and time
of the season. In great tits, fledging typically occurs in a period
with declining food resources (i.e., after the peak of caterpillar abundance, there main food resource; Matthysen et al.
2011). We predicted that for families breeding late in the
season and/or occupying low-quality territories, the lower
availability of food resources induces families to undertake
large-scale movements, offsetting the costs of moving around
with vulnerable offspring that may be risky in terms of predation and costly in terms of energy expenditure. Second, we
examined whether movement behavior reflects intraspecific
variation in reproductive strategies depending on parental
characteristics by relating movement behavior to breeding
experience and personality type. To test for differences in
breeding experience, we looked at the behavior of parents
of different age categories (Newton 1989; Forslund and Part
1995). As a measure of personality variation, we used exploration behavior during a novel environment test (Verbeek
et al. 1994; Dingemanse et al. 2002). Exploration behavior
has been shown to correlate with other behavioral traits such
as aggressiveness and risk-taking behavior and is often used as
a proxy to describe variation in animal personality (Reale et al.
2007). Third, we tested the hypothesis that movement behavior depended on previous experience with the local environment by comparing movements of families escorted by
first-year and older breeders, immigrant and locally fledged
birds. In addition, we tried to relate family movements to
areas previously used by the parents, by using information
on previous captures and observations.
MATERIALS AND METHODS
Study population and general field methodology
The study was conducted from 2007 to 2009 in a small-scale landscape with scattered woodland fragments called ‘‘the Boshoek’’
in northern Belgium (518080 N, 48320 E). This area of approximately 10 km2 consists of 17 woodlots of mature forest ranging
in size from 1 to 12 ha. Neighboring woodlots are 100–600 m
apart and separated by small residential areas and agricultural
land. Since 1993 all forest woodlots are equipped with standard
nest-boxes (height 1.5 m, dimensions 23 3 9 3 12 cm, entrance
32 mm) at a high density of about 6per hectare, containing
virtually the entire breeding population inside the woodlots
(for more details, see Nour et al. 1998; Matthysen 2002).
Each year during the breeding season (April–June), all nestboxes are checked weekly to determine the date of the first
egg laid (laying date), total number of eggs produced (clutch
size), and the total number of nestlings and fledglings. Parents are captured when their nestlings are 8–10 days old
and ringed with metal and color rings. Nestlings are ringed
when they reach a development stage equivalent to an age of
15 days which is used as a proxy for fledging date (Matthysen
et al. 2011). At this date, body weight and tarsus length are
measured. Additional captures are performed throughout the
year including mist net captures at feeders and nest-box controls for roosting birds. Standard measurements (weight, tarsus length) are taken at all times and birds not banded in the
nest are considered immigrants.
Exploratory behavior
Since 2006, we have routinely screened great tits on their
exploratory behavior using a novel environment test, following the exact procedure described in Dingemanse et al.
(2002). To briefly summarize: birds caught in the field
(July–February) were brought to the laboratory and kept in
individual cages for one night. The next morning, each bird
was entered separately into a sealed room (4.0 3 2.4 3 2.3 m)
containing 5 artificial trees, and during the following 2 min,
all movements among the different artificial trees (flights)
and among the branches of individual trees (hops) were
counted, including movements toward and from the lamps,
sliding doors or the floor, but not including movements on
a single branch. The sum of all movements was used as
a measure of exploratory behavior. All birds were released
near their site of capture within 24 h after capture. The
exploration score is repeatable (n ¼ 224, r ¼ 0.42, in resubmission Dingemanse et al. 2011). Because exploration
scores increase from summer to the start of the breeding
season, we corrected the scores for date of capture based on
within individual changes in behavior with capture date (for
details, see Dingemanse et al. 2002).
Postfledging space use of families
Spatial behavior of the families was determined by means of
radio tracking. Toward the end of the nestling phase when
nestlings were about 17 days old, we captured parents with
nest-box traps or mist nets and fitted either the male (2007–
2008) or the female parent (2009) with radio-tags. To attach
the radio-tag (transmitter case: 16 3 6 3 4 mm, antenna:
7 cm) to the birds, a backpack harness from stretch cord was
used with a span of approximately 43–45 mm (for details see
Naef-Daenzer 2007). The weight of the radio-tags was 0.75 g
(4% of the average body mass) and the tags lasted for
35–45 days (Model 1035, Advanced Telemetry Systems, Isanti,
MN). We located the birds on average 2 times per tracking day
(range 1–8 locations) between 7:00 and 21:00 with a time interval of at least 1 h. After locating the parent, we visually
confirmed whether the fledglings were present as nestlings
of focal broods were provided with brood-specific combinations of color rings at day 15. When families were foraging
high in the canopy, the presence of fledglings was determined
by auditory cues (i.e., begging or parental alarm calls). Families
usually forage separately from each other (van Overveld T,
van Overveld et al.
•
Postfledging family space use in great tits
personal observation, see also Naef-Daenzer and Gruebler
2008) and misidentification of begging is therefore unlikely.
Twice a week we located the roosting sites of all families and in
case families made large-scale foraging trips, we performed
additional checks to determine whether families changed
their roosting site or not.
Data analysis
Family space use
Postfledging space use by family groups was quantified by core
areas and home ranges, estimated by the fixed kernel contour
method using RANGES7 software (Anatrack Ltd; http://www.anatrack.com). For estimations of core areas, we used the contours of 50% of the location distribution with the highest use
density (50% kernel density estimate, KDE), and the total home
range was estimated by the contours of 95% of the total location
distribution (95% KDE). In order to compare ranging behavior
between families, we standardized our range calculations by using a constant kernel width for each family instead of using automated methods for smoothing factor selection (e.g., Wand and
Jones 1993). We chose to set the width around each point location (i.e., kernel width) to 50 m following Naef-Deanzer and
Gruebler (2008), as this probably most accurately reflects the
likelihood of presence of great tits.
Besides 2D estimates of ranging behavior, we more specifically looked at patterns of space use by calculating the distance
between the nest-box of origin and each location point, which
allowed us to study changes in space use over time and to
quantify variation in large-scale foraging excursions outside
the breeding woodlot (see Figure 1). We first calculated per
family, the average daily distance traveled, the median of the
maximum daily distance traveled, and overall maximum distance traveled during the postfledging period. Because all
measures were highly intercorrelated (Pearson correlation,
.0.85, P , 0.001), we used maximum distance traveled
as a proxy to describe the overall spatial extent of family
movements. Although maximum distance can be expected
to correlate strongly with home range estimates, this is not
necessarily true for families having multiple foraging areas.
In particular, we found this correlation to be strong for fam-
Figure 1
Examples of postfledging family movements of great tits with (A)
four families that remained in their fragment and (B) three families
that made excursions outside the natal fragment. Flags represent the
breeding nest-box and lines around locations family home range
sizes based on 95% KDE. Core areas and/or home ranges from
families in panel B showed a multimodal distribution with separate
foraging areas outside the breeding woodlot.
901
ilies not leaving their breeding woodlot (Pearson correlation,
r . 0.65, P , 0.005, n ¼17, for both core area and home
range) but weak for families making large-scale foraging excursions outside the woodlot (Pearson correlation, r . 0.38,
P . 0.2, n ¼ 15, see also Figure 2). Thus, in addition to other
measures of ranging behavior (core area and home range), we
consider maximum distance traveled as an additional independent measure of space use.
We found that variation in space use was to a large extent due
to some families, but not others, regularly undertaking foraging excursions outside the breeding woodlot. We defined families with excursions as those with core areas and home ranges
showing a multimodal distribution with a separate foraging
area outside the breeding woodlot (visually checked using Arcview3.1, see results for detailed description and Figure 1). Note
that we refer to these movements as ‘‘excursions’’ because all of
these families, with the exception of 2, returned to the natal
territory in the evening to roost. These excursions usually
lasted for the whole day with a minimum of at least several
hours (41). Families never undertook more than a single
excursion per day and often moved in the same general direction to the same specific area on different days. To quantify
excursion behavior, we took the total number of days on
which excursions outside the woodlot were observed. For
the analyses, we used daily excursion probability, that is, the
amount of time spent outside the breeding woodlot measured
by the number of excursion days relative to the total number
of tracking days. Space use was thus quantified by 4 different
variables: 1) core areas, 2) total home ranges, 3) maximum
distance traveled, and 4) daily excursion probability.
Explanatory variables
To test whether family space use varied with the quality of the
breeding territory, we calculated the average nestling body mass
per focal nest-box from 1993 to 2006, excluding the data from
the focal brood itself. We included first-broods only and to avoid
pseudoreplication due to females breeding in the same nest-box
for multiple years, we used the average nestling mass per female
and averaged this over females using a particular nest-box. For
one nest-box, no data were available because it was previously
only occupied by blue tits. We did not include data on the focal
Figure 2
Relationship between home range size and maximum distance
traveled from the nest-box for families that stayed within their
woodlot (filled symbols) and those that made excursions outside the
woodlot (open symbols). Squares indicate pairs with an adult female
parent and circles pairs with a 1-year-old mother.
Behavioral Ecology
902
brood to keep our measure of nest-box quality independent
from parental effects. Nest-box-specific average nestling mass
declined with the average timing of broods in the same nestbox, measured by the relative fledging date (deviation from the
annual mean, Pearson correlation, r ¼ 20.41, P ¼ 0.02, n ¼ 31).
We therefore consider our measure of nest-box quality to
represent components of both food availability and early breeding. We nevertheless included relative fledging date of the focal
brood to specifically test for effects of date because time of the
season may not only be important in terms of food but also with
respect to the opportunity of producing a second clutch. Great
tits are facultative multiple breeders with early breeders being
more likely to produce a second clutch (e.g., Verhulst et al.
1997), which in turn may influence the willingness to leave
the breeding territory (cf Rivera et al. 2000). To test the hypothesis that movement behavior depended on characteristics of the
parents, we included measures reflecting breeding experience,
familiarity with the study area, and personality. As a proxy for
breeding experience, we used age and distinguished between
1-year old (inexperienced breeders) and adult (experienced
breeders, i.e., . 1 year old). As a measure of familiarity with
the study area, we used dispersal status and distinguished
between locally born (individuals born in their breeding woodlot), dispersers (individuals born within the study population
but breeding outside their natal woodlot), and immigrants
(individuals from outside the study population; cf. Snoeijs
et al. 2004). As a measure of personality variation, we used
exploration score measured by the novel environment test
(see Material and Methods). In case we had multiple exploration scores for the same individual, we used the exploration
score when tested for the first time.
Statistical analyses
All analyses were performed using SAS 9.2 software. For 32 of 41
tracked families, we obtained data covering the complete
period of postfledging care, which lasted from 10 to 26 days.
We excluded data on 6 families with transmitter loss shortly
after fledging (,5 days, 4 due to predation and 2 to unknown
causes). We also excluded data from 3 families of which the
parents were predated on day 10, 11, and 13 because most
excursions occurred .10 days after fledging. On average, we
located the families 41 times (range 21–59), which is a relatively
small number of locations for home range calculations and
parts of the home ranges may therefore be missed (Nicholls
2005). Nevertheless, given that families with excursions typically moved to the same specific feeding areas on different days
and that the number of tracking days covered on average
85% of the total duration of the postfledging period (range
70–100%), we consider our data to give representative and
unbiased information on overall family movements.
Factors affecting core area size, home range size, and maximum distance traveled were analyzed using PROC MIXED
with Satterthwaite correction for the degrees of freedom
(df) (Littell et al. 1996). Normality of residuals was tested
using Shapiro–Wilk test and all dependent variables were
transformed as log10 (x 1 1) to improve normality of residuals. We analyzed factors affecting excursion behavior (daily
excursion probability) using PROC GLIMMIX with a binomial
link function. Because families were tracked in 3 fragments
differing in size and over 3 different years, we included woodlot and year as random terms in all models. The random
effects were nonsignificant in all models (likelihood ratio test,
P . 0.3). We ran separate models for analyses involving male
or female parental characteristics due to unequal sample sizes
of known exploration scores for males (n ¼ 32) and females
(n ¼ 25). The latter is due to our initial focus on the male
parent in the first 2 years of the study. Because we expected
families breeding closer to the edge of the woodlot to be more
likely to leave the woodlot, for the same degree of mobility, we
included a covariate representing this variation. Because of
the irregular shape of the woodlots, we chose to use the area
covered by forest within a radius of 75 m around the nest-box
as a representation of proximity to the edge. Model selection
was based on stepwise removal of nonsignificant fixed effects
starting from a full model, including all explanatory variables.
Because we had no a priori hypothesis for possible interactions between our covariates, we only tested for interactions
when analyses revealed that ranging behavior differed between age-categories and between families with or without
excursions.
Additional data analyses
We used an independent set of previously obtained visual observations on family movements as a confirmation of the results
obtained from radio tracking data. These observations were
recorded in 1996–2002 by intensive searches of the study area
(including the matrix between woodlots) for families with
color-ringed fledglings (details in Matthysen et al. 2010). These
observations resulted in a data set of 635 observations from 283
different families. Because of the incomplete and highly variable information per family, we did not calculate home-range
sizes or summary statistics of movements per family. Instead, we
used observation as an independent data point (or in case of
multiple observations of the same family on the same day, the
most distant one) and included family identity as a random
effect, in addition to year and study plot. In a first analysis, we
tested variation in distance (log-transformed as above) using
PROC MIXED. Explanatory variables were the same as in the
previous analysis except for exploration score, which was not
available for these years. Parental identities were not always
fully known which resulted in some missing data. We also
added brood age (days since fledging, including linear and
squared term) to the model in order to correct for the increase
in mobility with fledgling age. In a second analysis, we tested the
Table 1
Summary of differences in postfledging space use between families that remained in their breeding woodlot (no excursions) and families
making foraging excursions outside the breeding woodlot (excursions)
No excursions
Mean 6 SD
Core area (ha)
Home range (ha)
Maximum daily distance (m)
Within woodlots only
Excursions only
Maximum distance traveled (m)
0.93
2.90
92
92
6
6
6
6
0.58
1.79
41
41
180 6 58
Excursions
Range
N
Mean 6 SD
0.18–2.33
0.63–6.69
46–192
46–192
17
17
17
17
53–264
17
1.92
7.01
270
94
604
729
6
6
6
6
6
6
0.74
3.19
164
33
224
338
Range
N
0.78–3.24
3.37–15.2
102–616
45–152
290–989
346–1440
15
15
15
15
15
15
van Overveld et al.
•
Postfledging family space use in great tits
likelihood of leaving the fragment, with a distance of 75 m
outside the fragment border as a threshold, using PROC GLIMMIX with the same explanatory variables and random effects.
We repeated this analysis with other threshold distances
(25, 150 m) but found qualitatively similar results (details not
shown).
RESULTS
Space use and excursion behavior
903
Parental characteristics and family space use
We found that pairs with a 1-year-old mother had much higher
daily excursion probabilities compared with pairs of which the
mother was adult (F1,25.5 ¼ 17,59, P , 0.001, b 6 SE ¼ 1,72 6
0.41, see also Figure 2). As a consequence, these families moved
over larger distances (F1,30 ¼ 8.09, P ¼ 0.008, b 6 SE ¼ 0.34 6
0.12) had larger core areas (F1,30 ¼ 8.93, P ¼ 0.006, b 6 SE ¼
0.15 6 0.05) and total home ranges (F1,30 ¼ 5.39, P ¼ 0.027, b
6 SE ¼ 0.20 6 0.08). For families that remained in the breeding
woodlot, maternal age was not related to core areas or home
ranges (both P . 0.1). We found no effect of male age on family
space use (P . 0.9 in all models) nor did we detect any effects of
dispersal status (all P . 0.1). For summary of parental effects on
home ranges, see Table 2.
Postfledging space use differed considerably among families
with core areas ranging between 0.3 and 3.3 ha (median
1.5 ha) and home ranges between 1 and 15.2 ha (median 5
ha). The average maximum distance traveled varied from 75
to 1440 m (median 262 m). These distances largely exceed the
average territory size in our population, which based on
a breeding density of 3–4 pairs per hectare in the years of the
study, have an estimated diameter of about 60 m. All families
thus moved outside their breeding territory. The most striking
difference among families was the variation in the frequency
and extent of excursions outside the breeding woodlot
(Table 1), which we observed in 15 of 32 families (46%).
Average maximum distance traveled within the woodlot was
similar for families with and without excursions (95 and 91 m,
respectively), but when leaving the woodlot, families moved
on average from 236 up to 1440 m. As a consequence, families
undertaking excursions had larger core areas (F1,30 ¼ 21.18,
P , 0.001, b 6 standard error [SE] ¼ 20.18 6 0.04) and total
home ranges (F1,30 ¼ 27.05, P , 0.001, b 6 SE ¼ 20.31 6
0.06), although there was some overlap in range use between
the 2 groups (Table 1, Figure 2). The average number of
excursion days was 4 (range 1–12), corresponding to an average daily excursion probability of 25% (range 5–60%, n ¼ 15).
The earliest foraging excursion per family varied from day 3
to day 19 after fledging, with an average of 9.9. Excursions
were not necessarily made on consecutive days. None of the
measures of movement behavior differed between woodlots or
between years (generalized linear modal [GLM] all P . 0.1).
Area covered by forest within a radius of 75 m around the
nest-box also did not show an effect on family movement
behavior (GLM, all P . 0.8), and this variable was excluded
in further analyses.
From a total of 23 pairs with 1-year-old mothers, 14 families
made at least 1 excursion (61%), whereas for pairs with adult
mothers, only 1 pair of 9 made excursions (11%), which
differs significantly from a proportional distribution (chisquare ¼ 6.44 df ¼ 1 P ¼ 0.011). Within the group of families
with 1-year-old mothers, we found an additional effect of personality (see Table 2 for interaction age 3 exploration), with
more explorative mothers having larger core areas (F1,17 ¼
6.00, P ¼ 0.026, b 6 SE ¼ 0.20 6 0.08, Figure 4a) and total
home ranges (F1,17 ¼ 4.70, P ¼ 0.045, b 6 SE ¼ 0.01 6 0.00),
but no relationships were found with maximum distance traveled (F1,17 ¼ 0.22, P ¼ 0.64, b 6 SE ¼ 0.00 6 0.01). We
expected the larger range use by fast exploring 1-year-old
mothers to result from large-scale foraging excursions, but
maternal exploration score and excursion probability were
unrelated (F1,17 ¼ 2.45, P ¼ 0.14, b 6 SE ¼ 0.02 6 0.03).
However, 2 families with explorative mothers, but without
any excursions strongly affected the outcome of this analysis,
that is, when excluding these families, maternal exploration
was a strong predictor of daily excursion probability (F1,15 ¼
42.12, P , 0.001, b 6 SE ¼ 0.20 6 0.03, Figure 4b). Because
the fathers of these families were fitted with a radio-tag (2007/
2008), we checked the possibility that these mothers were
predated, but both were recaptured while breeding the
following season.
Environmental effects on family space use
Direction of excursions
Space use was unrelated to fledging date (P . 0.4 in all models, see
also Table 2) but differed between families from high- and lowquality territories. Families from low-quality territories were much
more likely to make large-scale foraging excursions (F1,29 ¼ 9.04,
P ¼ 0.005, b 6 SE ¼ 20.89 6 0.30), which resulted in negative
correlations between territory quality and both core areas
(F1,29 ¼ 5.31, P ¼ 0.029, b 6 SE ¼ 20.3 6 0.06) and home ranges
(F1,29 ¼ 3.37, P ¼ 0.077, b 6 SE ¼ 20.17 6 0.10), but not with
maximum distance traveled (F1,29 ¼ 2.03, P ¼ 0.17, b 6 SE ¼
20.20 6 0.14). Further analyses revealed that the relationship
between territory quality and space use differed between families
that either left or remained within the breeding woodlot (as shown
by significant interactions between territory quality 3 excursion
(yes or no) in all 3 models (P , 0.05), see also Table 2, Figure 3).
For families remaining in their woodlot, negative correlations
were found between quality of the territory and core areas
(F1,14 ¼ 12.44, P ¼ 0.003, b 6 SE ¼ 20.19 6 0.05), home ranges
(F1,14 ¼ 11.64, P ¼ 0.004, b 6 SE ¼ 20.30 6 0.09, Figure 2), and
maximum distance traveled (F1,14 ¼ 8.57, P ¼ 0.011, b 6 SE ¼
20.18 6 0.06). For families that left the breeding woodlot, no
relationships were found between territory quality and measures
of space use (P . 0.2 for all 3 variables).
To examine whether excursions were directed toward areas the
parents had visited before the breeding season, we looked at
locations of parents in the previous spring and summer outside their breeding woodlot. From the total of 15 pairs that
made at least one excursion, we had at least one such location
for 8 fathers and 11 mothers (7 pairs). These data included
the natal nest-box, radio tracking, mist net captures, and
passive transponder registrations. Due to low sample sizes,
we performed no statistical analyses.
For female parents, 7 of 11 excursions seem to be directed
toward previously visited areas, which are visually illustrated in
Figure 5. The direction of families b-c-d matched closely with
first-summer observations, especially when taking into account that these locations were up to 700 m or more away
and families had to cross open fields or use sparse vegetation
in order to reach them. The movements of families e-f-g-h
were less extreme and did not involve crossing open areas.
In the 4 remaining cases, we found no match, but these
included 2 cases where only the birthplace was known.
For male parents, 4 of 9 excursions showed a match with
previously visited areas. Two of 4 of these excursions were
made by the same male, but with a different partner (5.c
Second year female pairs and excursion behavior
Behavioral Ecology
904
Table 2
Final results of Generalized Linear Mixed Model on effects of territory quality, time of season, and parental characteristics on home range sizes
Mothers (n ¼ 24)
Exploration score
Dispersal status
Age
Season
Territory quality
Distance to edge
Excursion
Age 3exploration score
Excursion 3territory quality
Fathers (n ¼ 30)
df
F
P
b 6 SE
16.8
16.6
17
13.9
17
13.6
16.5
15.3
16.5
0.12
0.02
10.21
0.00
3.65
0.03
5.39
12.32
5.96
0.73
0.66
0.005
0.99
0.40
0.86
0.033
0.003
0.026
20.01
0.02
20.38
20.00
0.01
20.013
25.08
0.02
0.32
6
6
6
6
6
6
6
6
6
0.004
0.05
0.12
0.01
0.07
0.07
2.18
0.01
0.13
df
F
P
b 6 SE
21
24
24.4
23
26
22
26
0.08
1.14
1.88
0.52
2.84
0.45
8.27
0.78
0.29
0.18
0.47
0.10
0.51
0.008
0.00 6
0.08 6
0.07 6
20.016
0.08 6
20.04 6
26.8 6
26
9.15
0.005
0.00
0.05
0.05
0.01
0.09
0.06
2.0
0.38 6 0.12
Analyses were performed for mothers and fathers separately due to unequal sample sizes because of unknown exploration scores of some
mothers. Year and area were included as random effects in both models. Only significant interactions are shown.
and 5.e). The latter excursions were in a similar direction, but
the maximum distance traveled differed considerably (347 vs.
918 m). For the 5 cases that did not show a match, we had
captures of the male within the fragment used for breeding
the following year, but no captures outside this fragment.
From the 7 pairs for which we had locations of both parents,
only in one case both male and female were trapped at the
same summer location.
fects of time since fledging (F1,603 ¼ 5.14, P ¼ 0.024) and
nearness to the woodland edge (F1,312.6 ¼29.63, P ,
0.0001), and a significant effect of female age (F1,199.3 ¼
5.13, P ¼ 0.025), but no effect of territory quality (P . 0.4).
Analysis of visual observation data
The analysis of the visual observations collected in 1996–2002
showed that distance from the natal nest-box increased in
nonlinear fashion with time since fledging (Table 3). Families
born close to the woodland edge also traveled longer distances. The analysis confirmed that families with young mothers
were observed at larger distances (P ¼ 0.03; Table 3); however,
we did not find any effects of territory quality (P . 0.3,
Table 3). The same result was found in the analysis on the
likelihood of leaving the natal fragment, with significant ef-
Figure 3
Relationship between territory quality as measured by average body
mass of broods produced between 1993 and2006 and home range
size of families after fledging. Open dots represent families that left
their breeding woodlot and filled dots families that remained within
the breeding woodlot. Note that families leaving the breeding
territory had on average lower quality territories than families that
remained in the woodlot.
Figure 4
Relationship between exploration score of the mother and (a) home
range size (Exponential Rise to Maximumcurve, r2 ¼ 0.55, P ¼ 0.016)
and (b) excursion probability (Sigmoid curve, r2 ¼ 0.85, P , 0.001).
Open dots represent 2 families of which the mother had high
exploration scores and with relatively high home ranges, but without
excursions.
van Overveld et al.
•
Postfledging family space use in great tits
905
Figure 5
Foraging excursions of families
outside the breeding woodlot
in relation to known locations
of the female parent in her
first year (data on 1-year-old
mothers only). Crosses represent the natal nest-box and
filled dots summer locations
obtained by captures or registrations at feeders, except
d and h which were obtained
through radio tracking (d ¼
first summer and h ¼ postfledging period). Panel a shows
the study area. Maximum distances traveled during the
postfledging period are presented for each family. Family
movements shown in panel b–
h match with spring/summer
locations of the female parent,
whereas in i–l, there is no such
match.
DISCUSSION
We show that great tit families vary strongly in space use and
that this variation is related to both environmental factors
(territory quality) and parental characteristics (maternal
breeding experience and personality). Large-scale movements
outside the breeding fragments appeared to be daily excursions and not permanent shifts of the family range, in contrast
to a previous study on great tits (Drent 1984). Areas visited
during these long-distance excursion matched surprisingly
well with previously visited areas by the mother in several
cases, suggesting familiarity with the environment to play an
important role in patterns of space use. All together, these
findings support the idea that variation in family movements
reflects different parental care strategies to cope with
variation in food availability.
Our finding that families from low-quality territories were
more likely to make large-scale foraging excursions supports
our hypothesis that family movements are driven by the acquisition of new food resources and confirms the general notion
Table 3
Results of Generalized Linear Mixed Model of effects of territory
quality, time of season, and parental characteristics on family
movements using 635 observations of 283 families collected
between 1996 and 2002
Variables
df
F
Fledging age
(Fledging age)2
Male dispersal status
Female dispersal status
Male age
Female age
Season
Territory quality
Distance to edge
547
559
230
231
244
237
290
244
248
20.93
33.69
0.52
1.74
0.50
4.66
2.99
0.99
10.06
P
<0.0001
<0.0001
0.59
0.18
0.48
0.032
0.085
0.32
0.002
b 6 SE
0.09
20.002
20.05
0.07
20.03
0.1
0.011
0.04
20.013
6
6
6
6
6
6
6
6
6
0.01
0.00
0.05
0.05
0.05
0.05
0.006
0.04
0.07
Family identity was included as a random effect, in addition to year
and study plot.
that food conditions have profound effects on patterns of
space use in most birds and mammals (review in Boutin
1990). Our study further revealed a strong seasonal component in patterns of space use which can be explained by the
general changes in food availability. Great tits have been
shown to time their reproductive decisions such that the nestling phase of the young coincides with the seasonal peak in
caterpillar availability (van Noordwijk et al. 1995; Matthysen
et al. 2011). As a consequence, young fledge in a period in
which food resources are strongly declining. First, we found
that after fledging home ranges were much larger compared
with the average size of breeding territories, indicating that
parents had to cover larger areas in search for food compared
with the nestling period. Second, at the level of individual
territories, parents occupying high-quality territories were also
early breeders, indicating that besides the benefit of a general
good quality territory, these families may also profit from entering an environment in which food availability is still relatively high. Furthermore, because caterpillar densities usually
vary greatly among individual trees, resulting in a highly
patchy distribution of food resources (Fischbacher et al.
1998), fledging early may even provide an additional advantage by allowing families to move to unexploited food patches
less far away.
Our findings that family space use correlated with characteristics of female parents (particularly age) strongly contrast with
qualitative observations by Drent (1984), who suggested that
family movements are under paternal control, with movements being directed toward areas the male parent had visited
before. We do not know why movement strategies vary among
populations depending on parental sex or more general, why
movement strategies seem to be sex-specific, especially because both parents were usually found to be present at long
distance foraging excursions.
Although breeding experience is widely considered to be
a major component of variation in reproductive performance
(Forslund and Part 1995), we are not aware of other studies
reporting on effects of breeding experience on postfledging
parental care. At first sight, it appears counterintuitive that less
experienced birds are actually more likely to travel over large
Behavioral Ecology
906
distances with their offspring. However, we hypothesize that the
effect of experience is not so much the result of differences in
foraging or parental care skills but reflects a change in the
availability and use of information on the environment. We
suggest that, while experienced birds can rely on information
on locally available food resources collected in previous breeding attempts, inexperienced breeders lack such information
and therefore are more likely to rely on information they collected as first-summer bird in the previous year. When food
becomes scarce and birds may be forced to switch to different
types of prey and/or foraging locations, inexperienced birds
may therefore be more likely to move to distant foraging areas
of which they have prior knowledge. This hypothesis is supported by a number of striking examples of inexperienced
mothers moving toward previously visited areas. Our results
therefore highlight the possible role of information gathering
and long-term memory on space use in a bird species with
widely varying home range sizes in the course of the year. Great
tits are known to have much larger home-ranges in the nonbreeding compared with the breeding season (Drent 1984;
Matthysen 1990), and even in the nestling phase, excursions
outside the breeding territory have been observed (NaefDaenzer 1994). An unsolved problem, however, is why there
is no such effect of male breeding experience.
Within the group of inexperienced females, we found additional effects of female personality on space use with more explorative females covering larger areas and being more likely to
make daily large-scale foraging excursions. These findings fit
an emerging trend in studies on behavioral syndromes or
personalities, showing that proactive individuals (e.g., explorative, bold, and aggressive) have active foraging strategies
(Wilson and McLaughlin 2007; Herborn et al. 2010) and/or
move over larger distances (Fraser et al. 2001; Boon et al.
2008; Boyer et al. 2010). Moreover, we show that this difference is expressed in foraging behavior during a period that is
especially critical for survival of offspring, and hence like
mediates fitness variation among individuals (Gruebler and
Naef-Daenzer 2010).
Interestingly, we previously showed in the same population
that more explorative individuals responded to the experimental removal of food by a rapid change to different foraging areas
at larger distance from the feeding stations (van Overveld and
Matthysen 2010). We previously suggested that these different
responses resulted from personality differences in the use of
environmental information (cf. Benus et al. 1990; Drent and
Marchetti 1999), whereby fast explorers seem to rely more on
information from the past, whereas slow explorers use information in their current environment. The family excursion behavior on which we report here showed similarities with such
responses as more explorative mothers left the vicinity of the
breeding territory relatively quickly (and thus more often) with
some strong examples of long-distance movements being directed toward places on which the mother had prior knowledge. The fact that personality effects were expressed only in
inexperienced female parents fits the idea that certain personality traits may only become visible when individuals face challenging situations (Reale et al. 2007).
Finally, our results provide some support for the previously
suggested hypothesis that the relationship between parental
exploration behavior and natal dispersal distances of the
offspring may at least partly depend on personality differences in space use during the period of postfledging care
(Dingemanse et al. 2003; Matthysen et al. 2010). On the other
hand, the fact that personality effects on family space use were
age and sex specific suggests this effect to be rather weak.
Overall, our study nevertheless shows that fledglings may differ greatly in the types of environmental information they
receive in the early stages of life, which appears to depend
on both environmental factors and parental characteristics.
These findings may provide new directions to study the effects
of early experience and parentally transmitted information on
spatial behavior in animals with extended parental care.
We thank Frans Fierens and Joris Elst for collecting general field data
and Tom van de Casteele, Hans Matheve, and Diederik D’Hert for
collecting visual observations on family movements. We are grateful
to Niels Dingemanse, Beat Naef-Daenzer, and an anonymous referee
for their helpful comments on a previous version of the manuscript.
Financial support was received by an FWO-Flanders doctoral fellowship
to T.V.O. and a BOF-NOI grant from the University of Antwerp to E.M.
This study complies with legal requirements for research in Belgium.
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