Journal of Animal
Ecology

2007

76

, 915–925

© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society

Blackwell Publishing LtdAge-related change in breeding performance in early life is
associated with an increase in competence in the migratory
barn swallow

Hirundo rustica

JAVIER BALBONTÍN*, IGNACIO G. HERMOSELL*, ALFONSO
MARZAL*†, MARIBEL REVIRIEGO*, FLORENTINO DE LOPE* and
ANDERS PAPE MØLLER‡

*

Departamento de Biología Animal, Universidad de Extremadura, E-06071 Badajoz, Spain;

†

Department of Animal
Ecology, Ecology Building, Lund University, S-223 62 Lund, Sweden; and

‡

Laboratoire de Parasitologie Evolutive,
CNRS UMR 7103, Université Pierre et Marie Curie, Bât. A, 7ème étage, 7 quai St Bernard, Case 237, F-75252 Paris
Cedex 05, France

Summary
1.

We investigated age-related changes in two reproductive traits (laying date and annual
fecundity) in barn swallows

Hirundo rustica

L. using a mixed model approach to di-
stinguish among between- and within-individual changes in breeding performance
with age.

2.

We tested predictions of age-related improvements of competence (i.e. constraint
hypothesis) and age-related progressive disappearance of poor-quality breeders (i.e. selec-
tion hypothesis) to explain age-related increase in breeding performance in early life.

3.

Reproductive success increased in early life, reaching a plateau at middle age (e.g. at
3 years of age) and decreasing at older age (

>

4 years). Age-related changes in breeding
success were due mainly to an effect of female age.

4.

Age of both female and male affected timing of reproduction. Final linear mixed
effect models (LME) for laying date included main and quadratic terms for female and
male age, suggesting a deterioration in reproductive performance at older age for both
males and females.

5.

We found evidence supporting the constraints hypothesis that increases in com-
petence within individuals, with ageing being the most probable cause of the observed
increase in breeding performance with age in early life. Two mechanisms were
implicated: (1) advance in male arrival date with age provided middle-aged males with
better access to mates. Yearling males arrived later to the breeding grounds and therefore
had limited access to high-quality mates. (2) Breeding pairs maintaining bonds for 2
consecutive years (experienced pairs) had higher fecundity than newly formed
inexperienced breeding pairs.

6.

There was no support for the selection hypothesis because breeding performance
was not correlated with life span.

7.

We found a within-individual deterioration in breeding and migratory performance
(arrival date) in the oldest age-classes consistent with senescence in these reproductive
and migratory traits.

Key-words

: breeding experience, constraints and selection hypothesis, fecundity, linear
mixed effect models (LME), longevity, senescence, timing of reproduction.

Journal of Animal Ecology

(2007)

76

, 915–925
doi: 10.1111/j.1365-2656.2007.01269.x

Correspondence: Javier Balbontín, Departamento de Biología Animal, Universidad de Extremadura, E-06071 Badajoz, Spain. E-
mail: jbalare@unex.es

916

J. Balbontín

et al.



© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,

Journal of Animal
Ecology

,

76

,
915–925

Introduction

Empirical studies of free-living vertebrates suggest
strongly that reproductive performance increases with
age, reaching a maximum output at middle age, fol-
lowed by a clear deterioration at advanced age due to
senescence (Clutton-Brock 1988; Forslund & Pärt 1995).
This association between age and fecundity has been
observed in fish (Hodder 1963), amphibians (Salthe
1969), reptiles (Tinkle & Ballinger 1972), mammals
(Clutton-Brock 1988) and birds (Newton 1989; Sæther
1990; Forslund & Pärt 1995). Three major groups of
non-exclusive hypotheses based on progressive appear-
ance or disappearance of individual phenotypes among
age-classes (delayed breeding and selection hypo-
theses; Perrins & Moss 1974; Curio 1983; Newton 1989),
age-related improvements of competence (constraint
hypotheses; Curio 1983; Nol & Smith 1987; Pärt 2001)
and optimization of reproductive effort (restraint hypo-
theses; Williams 1966; Pianka & Parker 1975; Clutton-
Brock 1988) have been proposed to explain the increase
in reproductive output with age in early life. It is impor-
tant to realize that changes in phenotypic traits could
result from within-individual patterns (e.g. ageing) and
from between-individual changes in the quality of
individuals entering or leaving the population (e.g.
selection). The constraint and restraint hypotheses
focus on the phenotypic changes that take place
within individuals, and the selection or delayed-
breeding hypotheses focus on phenotypic changes
among individuals.
The selection hypotheses assume that there is always
a difference in quality among individuals in a popula-
tion. The progressive disappearance of individuals with
poor reproductive performance occurs if such individ-
uals have lower survival probabilities than individuals
with superior reproductive success, and therefore a
positive correlation between reproductive performance
and survival or longevity is expected at the population
level. Although natural selection is involved in this
process, humans can cause mortality on cohorts that
reverse the pattern due to natural selection (Balbontín,
Penteriani & Ferrer 2005). Most studies have reported
associations between age and reproductive traits based
on cross-sectional comparisons. Because individuals
within a population differ in their ability to acquire and
utilize resources and in their optimal allocation of such
resources, between-individual variation in quality can
mask within-individual ageing patterns in cross-
sectional studies (Nol & Smith 1987; Forslund & Pärt
1995; Nussey

et al

. 2006; van der Pol & Verhulst 2006).
In particular, problems of estimating age-effects for
reproductive traits within individuals arise when there
is a difference in quality among individuals causing
a difference in longevity. Using longitudinal data on
reproductive traits of individuals over their lifetime, the
selection hypothesis could be tested readily. Recently,
van der Pol & Verhulst (2006) suggested that by using
linear mixed models appearance or disappearance
effects could be tested easily by adding age at first repro-
duction (appearance effects) or longevity (i.e. age at last
reproduction, disappearance effects) as a covariate in a
model in which age is kept as a fixed effect for investi-
gating their effects on reproductive traits. Correlations
between reproductive traits within individuals are
controlled by adding individual identity as a random
effect in these models.
The constraints hypotheses suggest that with increas-
ing age, individuals improve in skills that improve
reproductive performance. Many different ways of
increasing competence have been proposed. For instance,
a prolonged period of learning is needed to perform all
reproduction tasks correctly to raise healthy young
successfully. Therefore, previous breeding experience
has been suggested to influence breeding performance
positively. Increased experience while ageing could also
be due to learning to cope with predators or competi-
tors, familiarity with the local environment or within-
individual improvement in feeding behaviour, all of
which could cause an increase in reproductive output
with age (Burger 1988; Marchetti & Price 1989; Desro-
chers 1992). Other extrinsic mechanisms may prevent
young individuals from reproducing as successfully as
older individuals. For instance, improvement in breed-
ing success with age could be due to limited access to
high-quality mates or territories for young individuals.
Therefore, limited access to resources by young indi-
viduals due to constraints on migratory performance
or dominance status might cause poor reproductive
performance when young.
The restraint hypotheses suggest that individuals
enhance reproductive performance as they grow old
because of a decrease in residual reproductive value
(Williams 1966; Gadgil & Bossert 1970; Curio 1983;
Charlesworth 1994). Life history theory predicts a
trade-off between reproduction and survival or between
current and future reproduction (Stearns 1992). Assum-
ing such trade-offs, individuals may invest less in repro-
duction when young because they trade investment of
resources between current reproduction and survival
to the next breeding season.
Most studies of wild vertebrates failed to describe
the effect of age on fecundity in the last part of the life
of an individual. Studies rarely tested whether declines
in reproductive performance in later life are due to
changes in within- or between-individual performance.
Theories of senescence deal with within-individual
changes in reproductive performance with age. However,
when using cross-sectional data, changes in perform-
ance between individuals might mask patterns of senes-
cence in reproductive output. For example, if individuals
that increase reproductive effort in early life pay a cost
in terms of reduced longevity or accelerated repro-
ductive deterioration in late life, then the observed
pattern of reproductive senescence would be due to the
disappearance of high-quality breeders rather than
a phenotypic change within a given individual.
Therefore, separation of within- and between-individual

917

Breeding
performance in
early and late life
and age

© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,

Journal of Animal
Ecology

,

76

,
915–925

variation in age-related breeding performance consti-
tutes a major challenge for the study of senescence at
the population level in the wild (Forslund & Pärt 1995;
Nussey

et al

. 2006; van der Pol & Verhulst 2006).
Our main aim was to test hypotheses explaining age-
related increase in two reproductive traits (e.g. lay date
and annual fecundity) early in life, using the barn swa-
llow (

Hirundo rustica

L.) as a model species. The barn
swallow is a small (

c

. 20 g), socially monogamous, se-
micolonial passerine feeding on insect prey. It is a long-
distance migratory bird covering up to

>

10 000 km
between breeding and wintering sites. Barn swallows
breed on farms, gaining permanent access through
open doors and windows. Females lay between one and
three clutches containing one to six eggs per breeding
season. Breeding dispersal is very low, because less
than 0·1% of

>

10 000 banded adults (studied during
30 years in populations in Spain, Italy and Denmark,
including the population studied here) moved between
breeding colonies from one year to the next, and all but
one among 450 local recruits was captured in the first
year of life (Møller, de Lope & Saino 2005). Therefore,
age at first reproduction shows little or no variation,
with most individuals starting reproduction at the age
of 1 year. On average, only 35% of breeding individuals
survive to the next breeding season (Møller 1994a; Saino

et al

. 1999), with very few reaching very old age (i.e. 1·5%
of first-time breeding birds reached the age of 5 years).
None the less, longevity or age at last reproduction shows
considerable variation (range: 1–8 years) compared with
age at first reproduction, and therefore only disappear-
ance effects are likely to mask within-individual changes
in age-related fecundity in this short-lived species.

 

(

-
   
 

)

Selection: progressive disappearance hypothesis

Breeding performance increases with age because poor-
quality breeders die young. We predicted annual bree-
ding success to be correlated positively with longevity
(i.e. age at last reproduction) and negatively with lay
date. This association between age at last reproduction
and a reproductive trait (i.e. annual fecundity or lay date)
must hold when measuring breeding performance con-
trolling for age. This hypothesis assumes a difference in
quality between individuals with different life spans.
Long-lived individuals should be better breeders than
individuals with short life spans.

Constraint: breeding experience hypothesis

More experienced breeders or breeding pairs repro-
duce better than less-experienced breeders or breeding
pairs. Breeding experience should increase final repro-
ductive output. Because there is no variation in age at
first breeding, all similarly aged individuals should have
similar breeding experience, and therefore we used pair-
bond duration as an index of breeding experience. We
predicted breeding pairs maintaining bonds to repro-
duce better than newly formed breeding pairs. Because
improvement in competence occurs within individuals,
we controlled for between-individual changes by incor-
porating age at last breeding into the analyses when
testing this hypothesis.

Constraint: limited access to high-quality mates or
territories hypothesis

Improvement in breeding success with age is due to
limited access to high-quality mates or preferred nest sites
at younger ages. We predicted that migratory perfor-
mance (measured as the date that male and female arrived
at the breeding grounds) should decrease with age, at
least in early life. Early-arriving individuals should have
better access to mates and preferred nest site than late-
arriving ones. We assumed that early arrival provides
males and females with a greater advantage in terms of
mating success, laying date and annual reproductive
output than late-arriving individuals, as demonstrated
previously in several studies on this species (Møller
1994a,b; Saino

et al

. 1997; Kose & Møller 1999; Kose

et al

. 1999; Møller, de Lope & Saino 2004). Because
change in improvement in competence occurs within
individuals, we controlled for between-individual
changes by incorporating age at last breeding into
analyses when testing this hypothesis.
Finally, we tested whether deterioration in reproduc-
tive performance (laying date and annual fecundity)
and migratory performance (arrival date) in late life was
due to trade-offs between reproduction and survival by
introducing curvilinear relationships between age at
last reproduction and breeding performance, as doc-
umented previously in wild vertebrates (Reid

et al

. 2003).

Methods

 

We studied barn swallows at Badajoz, south-west Spain
(38

°

50

′

N, 6

°

59

′

W). The study site was mainly open
farmland with pasture, cereals and fruit plantations (de
Lope 1983). Early during the breeding season we cap-
tured adults at dawn by using mist nets across windows
and doors of the breeding sites. We studied barn swallows
in four different colonies: Potosi (POT), Almendral
(ALM), Tres Arroyos (TA), and Virgen de Guadalupe
(VG) within our study area (mean

±

SD distance between
colonies: 10781 m

±

8505, range: 1706–20 338 m). We
made weekly captures of birds during every breeding
season until 98–100% of breeding individuals were cap-
tured. Each bird was identified with a numbered metal
ring and a combination of coloured PVC rings, so we
could recognize each adult visually. We measured right
and left outermost tail feathers with a ruler to the nearest
0·5 mm. Tail length was determined as the mean value

918

J. Balbontín

et al.



© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,

Journal of Animal
Ecology

,

76

,
915–925

of left and right characters. Individuals with broken
tails were excluded from the analyses, because the rounded
tip of the outermost tail feathers reveals clearly whether
it is broken. Body mass was recorded with a Pesola
spring balance to the nearest 0·5 g. All measures were
taken by the same observer (F. de L.), which eliminates
any noise in the data due to interobserver variability.
All birds were provided with an individual combination
of colour markings on their belly feathers using stamp
ink. Individuals were sexed from the presence (females)
or absence (males) of a brood patch and from observa-
tion of breeding behaviour during the courtship and
incubation period.
We tracked all reproductive events and identified
visually each individual of pairs using binoculars from
inside a hide, to avoid disturbance during reproduc-
tion. We checked all nests in our colonies every 2 days
during the breeding season with the aim of recorded
laying date, clutch size and brood size up to the third
brood. Once females started laying we conducted daily
observation sessions inside a hide, observing each
occupied nest, with the aim of identifying individuals
based on colour rings and ink marks. We were able to
identify each individual in the pair and their nest for the
majority of the occupied nest sites. Because these po-
pulations have been subject to several experimental studies
(tail-length manipulation), we eliminated from our data
set any individuals involved in these experiments (89
manipulated males and 32 manipulated females). How-
ever, manipulated birds differed from non-manipulated
birds for several traits, resulting in a non-random subset
of individuals being involved in experiments. Females
involved in experiments arrived later [mean (SE):
–0·02 (0·05)], laid later [standardized lay date: –0·05
(0·05)] and had shorter tails [84·6 mm (0·30)] than non-
manipulated females [mean (SE), standardized arrival
date: –0·48 (0·08), standardized laying date: –0·48 (0·06),
tail length: 86·9 mm (1·10 mm)], and manipulated males
arrived later [mean (SE): –0·02 (0·05)] and were older
[mean (SE): 2·00 (0·06) years] than non-manipulated
males [standardized arrival date, mean (SE): –0·37
(0·06), age: 1·67 (0·09) years] (

t

-tests employed to check
for differences on tail length, standardized arrival date,
standardized lay date, standardized annual breeding
success and age). Because tail manipulation was per-
formed as birds arrived at our study areas, starting a
little later during the breeding season, it could result in
the sample of manipulated birds being skewed towards
later arrival date, which could explain the observed di-
fferences in arrival date, lay date, male age and tail length
between manipulated and non-manipulated individuals.
However, the sample of non-manipulated birds (i.e.
those used in the present study) encompassed the entire
range of the population for arrival date, tail length, lay
date and age. Therefore, excluding manipulated birds
would have reduced the number of later-arriving and
breeding individuals and the number of females with
shorter tails from our final samples. In total, we iden-
tified individual males and females for pairs for 322
breeding events during 1994–2006. Two different
measures of breeding success were employed. Annual
fecundity was measured as the total number of chicks
raised to fledging age every year (in up to three different
annual broods), and laying date was estimated as the
date of the first egg of the first brood, relative to day 1
(1 March). Migratory performance (arrival date) was
measured as the first day an individual was captured in
our consecutive capture–recapture sessions, relative
to day 1 (1 February). The precision of this estimate
has been checked previously by observations from the
beginning of the breeding season and calculating a
second measure of arrival date as the first day an adult
bird was identified from its colour rings and belly ink
marks. The correlation between these two estimates
was very high (Pearson’s correlation coefficient: range:
0·98–0·99, calculated in 7 different years for both sexes
separately; Møller

et al

. 2004).
Several studies have demonstrated that barn swa-
llows show high site fidelity and rarely leave the colony.
Therefore, disappearance of colour-ringed breeders from
the colony indicated mortality rather than dispersal.
Once a 1-year-old individual returned from its first
migration, it selected a breeding area and remained
loyal to it for the rest of its life. Therefore, we could
assign the age of individuals with accuracy in our study
colonies, assuming unringed birds to be yearlings at
first capture (Møller 1992; Møller

et al

. 2005).

 

We used linear models to investigate the effect of age on
breeding success and migratory performance. The key
feature of longitudinal data is that individuals are
measured repeatedly through time. Linear mixed effect
models (LME) are particularly useful when there is
temporal pseudo-replication (repeated measurement).
We used the LME procedure of S-Plus 2000 (Mathsoft
1999) to investigate the effect of age of the female and
its mate on breeding performance, timing of breeding
(lay date) and migratory performance (arrival date).
We controlled for interannual variation on breeding
and migratory performance by standardizing the first
egg-lay date, annual fecundity and arrival date by sub-
tracting the annual population mean from each observed
value and dividing by the annual population standard
deviation (Zar 1999). We used a normal error distribu-
tion with an identity link function to model standar-
dized arrival, first egg-lay date or annual fecundity as
response variables. Full and reduced models were
fitted by using a maximum likelihood (ML) method
and final parameters for final minimal adequate
model were estimated using the restricted maximum
likelihood (REML) method (McCullough & Nelder
1989; Crawley 2002). There was missing information
for some individuals, which resulted in slightly varying
sample sizes in different analyses.
Because of high adult mortality (

>

65%, Møller 1994a;
Saino

et al

. 1999) the duration of pair-bonds was always

919

Breeding
performance in
early and late life
and age

© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,

Journal of Animal
Ecology

,

76

,
915–925

short, and therefore we could not specify pair identity
as a random factor. Accordingly, when modelling
reproductive traits, we introduced bird identity (female
or female’s mate identity) as a random effect, incorpo-
rating identity of the female in a first attempt and there-
after repeating the analysis using identity of the female’s
mate, with the aim of checking if conclusions for fixed
effects were similar using these two different approaches.
Explanatory variables were female’s and mate’s age,
female’s and mate’s age at last reproduction (ALR)
(defined as the age a breeding individual was last
recorded in the breeding colony), colony (factor with
four levels, POT, ALM, TA and VG) and pair-bond
duration (i.e. the number of breeding seasons a pair
had bred together). We also fitted full models with
female’s and mate’s body mass (g) and female’s and
mate’s tail length (mm) when modelling standardized
laying date. Also, female’s and mate’s arrival and laying
date was included to model standardized annual fecun-
dity, because they have been shown previously to affect
these reproductive traits (review in Møller 1994a). When
the response was standardized arrival date (for either
males or females), explanatory variables introduced
into the models were age and ALR of either sex. All these
variables were treated as fixed-effects in all models.
The selective disappearance hypothesis was in-
vestigated following van der Pol & Verhulst (2006).
ALR was left in all models independent of its effect, in
such a way that we could test specifically for within-
individual age effects in the presence of a selective
disappearance effect (the estimated slope of ALR).
Investigation of the dispersion plots suggested incor-
poration of female’s and mate’s age as second-order
polynomials in a maximal model. Curvilinear relation-
ships between ALR and breeding performance were also
tested, because a significant effect could suggest
trade-offs between reproduction and survivals (Reid

et al

. 2003; Nussey

et al

. 2006). Therefore, we first
included second-order main fixed effects and possible
two-way interactions in a maximal model, reducing it
by eliminating non-significant terms from the fixed
structures (Crawley 2002). The statistical significance
of each covariate and all possible two-way interactions
among fixed effects were tested in turn, using a back-
ward stepwise procedure to select the most parsimoni-
ous model. Models with different fixed structures were
compared using

F

-tests, Akaike’s information cri-
terion (AIC) and L-ratio tests (Akaike 1973; Pinheiro
& Bates 2000; Crawley 2002). The final model was
considered to have been reached when all variables
(except ALR) had a significant effect at

P



<

0·05.

Results

      
 

The age of the two members of a breeding pair was
related to the start of breeding. LME showed that the
most parsimonious model included both main and
quadratic terms for the female and its mate’s age, while
accounting for the known source of variability due to
among-individual variation (Table 1). This model was
significant (L-ratio

=

95·91,

P



<

0·0001). Middle-aged
females (3 years) started incubation earlier than young
(1–2 years) and older females (4 years or older). The
age of the female mate’s was related to the start of
reproduction in a similar way. Females that mated
with middle-aged (3 years) males laid eggs earlier than
those mated with either young (1–2 years) or older mates
(4 years or older), independently of their own age
(Fig. 1). The interaction between female and male age
was not statistically significant. There was no effect
of disappearance of low-quality individuals (esti-
mated

β

s

for main and quadratic terms on female’s ALR:

P



>

0·2, Table 2). Female tail length was related to start
of reproduction, with long-tailed females starting to
reproduce earlier than the average females. The dur-
ation of the pair-bond was not related significantly to
the onset of reproduction (

P

>

0·2). Neither male
tail length nor male or female body mass were related
significantly to the onset of reproduction. There was
considerable between-individual variation in first-egg
lay date, with female identity accounting for 43% of
the total variance (calculated in a model without
fixed effects).

      


Only age of the female in the breeding pair was related
significantly to annual fecundity. The most parsimoni-
ous model retained main and quadratic terms of female
age, while accounting for the known source of variability

Table 1.

Linear mixed models of standardized first egg-lay date as the response
variable. Full models built with age and age at last reproduction (ALR) of female, pair-
bond duration, colony, age and ALR of female’s mate, female and male body mass and
tail length as explanatory variables. Only significant terms are shown, except for female
ALR, which was retained in the model. Sample size is 322 breeding events for known-
age breeding pairs
Random effects
SD 95% CI
Female identity 0·566 0·451–0·710
Residual 0·581 0·493–0·685
Fixed-effects
Estimate SE d.f.

F P

Intercept (

β

0

) 3·461 0·814 1, 234 0·00 0·96
Female age (

β

1w

) –0·663 0·158 1, 67 43·04

<

0·0001***
Female age

2

(

β

2w

) 0·087 0·026 1, 67 29·34

<

0·0001***
Female ALR (

β

3s

) –0·068 0·161 1, 67 0·00 0·95
Female ALR

2

(

β

4s

) 0·011 0·025 1, 67 0·07 0·77
Mate’s age (

β

5

) –0·771 0·150 1, 67 17·99

<

0·0001***
Mate’s age

2

(

β

6

) 0·113 0·027 1, 67 16·27 0·0001***
Female tail length (

β

7

) –0·019 0·009 1, 67 4·34 0·04

920

J. Balbontín

et al.



© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,

Journal of Animal
Ecology

,

76

,
915–925

due to among-individual variation (Table 2). The final
model was significant (L-ratio

=

21·57,

P



=

0·0014).
Average annual fecundity for middle-aged females
(3 years) was 6·74

±

2·95 fledglings/year, which was larger
than average annual fecundity of young females (1–
2 years, mean

±

SD

=

5·44

±

2·66 fledglings/year) or older
females (4 years or more, mean

±

SD

=

5·88

±

2·99
fledglings/year) (Fig. 2). Neither the effect of male age
nor the interaction between female and male age was
retained in the model. There was no significant effect of
disappearance of low-quality individuals (estimated

β

s

for main and quadratic terms on the female’s ALR:

P



>

0·4, Table 2). The duration of the pair-bond was
related significantly to final reproductive output. Thus,
the average annual fecundity of pairs that bred together
twice was significantly larger (mean

±

SD

=

7·32

±

3·03
fledglings/year,

n



=

19) than that of pairs that remained
together for just one breeding season (mean

±

SD

=

5·41

±

2·74 fledglings/year,

n



=

219, Fig. 3). Male body
mass was also retained in the final LME. Male body
mass was related positively to the number of chicks
fledged. Neither female (L-ratio

=

0·81,

P



=

0·36) nor
male arrival date (L-ratio

=

2·86,

P

= 0·09) or lay date
(L-ratio = 2·15, P = 0·14) were retained in the minimal
adequate model. However, if we excluded from the
full model the main and quadratic effects of female age,
the effect of laying date and arrival date become highly
significant (estimate ± SD: laying date = –0·184 ± 0·06,
L-ratio = 8·29, P = 0·004; female arrival date = –0·167
± 0·059, L-ratio = 7·77, P = 0·005; male arrival date = –0·182
± 0·05, L-ratio = 9·83, P = 0·001). Between-individual
Fig. 1. (a) Effect of female age on laying date; (b) effects of
mate’s age on laying date having accounted for female age
effect (i.e. mate’s age effect on residuals from the regression of
female age on laying date).
Fig. 2. Effect of female age on standardized annual fecundity.
Breeding females aged 1, 2, 3, 4, 5, 6 and 7 years old. Sample
size is 313 breeding events.
Fig. 3. Box plots for standardized annual fecundity for
experienced (i.e. breeding together for two consecutive years,
n = 19 breeding attempts) and inexperienced breeding pairs
(i.e. breeding together for just 1 year, n = 219 breeding attempts).
Table 2. Final linear mixed model obtained for standardized annual fecundity. Full
model fitted with female age, female age at last reproduction (ALR), pair-bond
duration, colony, age and ALR of female’s mate, male and female body mass and tail
length as explanatory variables. Only significant terms are shown, except for female
ALR, which was retained in the model. Sample size is 312 breeding events for known-
age breeding pairs
Random effects
SD 95% CI
Female identity 0·237 0·036–1·536
Residual 0·931 0·805–1·078
Fixed-effects
Estimate SE d.f. F P
Intercept (β0) –0·280 0·847 1, 203 0·20 0·65
Female age (β1w) 0·443 0·221 1, 66 3·58 0·06
Female age2 (β2w) –0·076 0·038 1, 66 7·35 0·008**
Female ALR (β3s) –0·045 0·183 1, 66 0·40 0·52
Female ALR2 (β4s) 0·012 0·027 1, 66 0·47 0·49
Pair-bond (β5) 0·532 0·239 1, 66 4·88 0·03*
Male body mass (β6) 0·097 0·043 1, 66 5·14 0·02*

921
Breeding
performance in
early and late life
and age
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
915–925
variation in annual fecundity (calculated for female
identity) accounted for 16% of the total variance (cal-
culated in a model without fixed effects).
     
 
Linear mixed models showed that age was related to the
date males returned to their breeding grounds. Variation
in male arrival date was best explained by a model inclu-
ding male age with significant main and quadratic terms,
while accounting for the known source of variation due
to among-male identity (Table 3). This model was sig-
nificant (L-ratio = 73·76, P < 0·0001). Middle-aged males
(3 years) arrived earlier than either young (1–2 years)
or older males (4 years or older) (Table 3, Fig. 4a).
There was no effect of disappearance of low-quality
individuals in early life (main effect of ALR, P > 0·2).
The quadratic terms of ALR were also not significant
(P = 0·21, Table 3). There was considerable between-
individual variation in male arrival date, with male
identity accounting for 33% of total variance (calcu-
lated in a model without fixed effects).
Age was related in a quadratic fashion to the day
females returned to their breeding grounds. The final
LME model included both linear and quadratic terms
for female age (L-ratio = 74·65, P < 0·001). Female age
was related to their arrival date at the breeding grounds
in a similar way to males, with an optimum age of arrival
at 3 years. Younger (1–2 years) and older females (4 years
or more) arrived later at the breeding grounds (Table 3,
Fig. 4b). There was no significant effect of disappear-
ance of low-quality individuals on the date of female
arrival [estimate (βs) for main and quadratic terms
P > 0·2; Table 3]. There was considerable between-
individual variation in female arrival date, with female
identity accounting for 40% of total variance (calcu-
lated in a model without fixed effects).
Discussion
The main findings of this study were (1) that annual
fecundity increased with age in early life, reaching a
maximum at mid-life and decreasing in late life; (2) the
association between breeding performance and age
was due mainly to a change in within-individual ageing
rather than to a change in between-individual pattern or
Table 3. Linear mixed models of standardized male and female arrival date as the response variable, and age and age at last
reproduction (ALR) as explanatory variables. Only significant terms are shown except for female ALR. Sample size is 319 and
320 arriving males and females, respectively
Standardized male arrival date
Random effects
Standardized female arrival date
SD 95% CI SD 95% CI
Male/female identity
Residual
0·405 0·223–0·736 0·491 0·306–0·790
0·802 0·688–0·935 0·807 0·682–0·954
Fixed-effects
Estimate SE F P Estimate SE F P
Intercept (β0) 1·741 0·245 0·10 0·74 0·750 0·222 0·06 0·80
Age (β1w) –1·070 0·200 36·40 <0·0001 –0·754 0·193 13·88 0·0004
Age2 (β2w) 0·158 0·035 32·77 <0·0001 0·113 0·033 11·32 0·001
ALR (β3s) –0·290 0·198 1·04 0·30 0·128 0·183 1·10 0·29
ALR2 (β4s) 0·038 0·030 1·55 0·21 –0·030 0·028 1·14 0·28
Fig. 4. (a) Effect of male age on standardized male arrival
date; (b) effect of female age on standardized female arrival
date. Curvilinear relationships (i.e. model prediction) are
shown. Sample size was 320 females and 319 males.

922
J. Balbontín et al.
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
915–925
selection; (3) the association between age and annual
fecundity was due mainly to a female age effect; (4) both
female and male age affected the timing of reproduction;
(5) two reproductive traits (i.e. annual fecundity and
laying date) and one migratory performance trait (i.e.
arrival date) deteriorated in late life; (6) between-
individual variation in individual phenotypic quality
did not affect change in migratory performance with
age; and we found that (7) some evidence supporting
‘constraints’ hypothesis were found because breeding
performance increases with breeding experience and
migratory performance improve while ageing. Each of
these main findings are discussed briefly.
Numerous empirical studies have established that
reproductive performance in birds generally improves
with age (Clutton-Brock 1988; Forslund & Pärt 1995;
Sanz & Moreno 2000; Green 2001; Pyle, Sydeman &
Hester 2001; Laaksonen, Korpimäki & Hakkarainen 2002).
However, the reasons for such increases are still poorly
understood. Experimental and observational studies
in birds and mammals have found evidence consistent
with the increase in competence and selection hypoth-
eses for explaining age-related fecundity in early life
(De Steven 1978; Desrochers 1992; Komdeur 1996;
Balbontín, Penteriani & Ferrer 2003; Ferrer & Bisson 2003;
Penteriani, Balbontín & Ferrer 2003). Reid et al. (2003),
in a review of the bird literature, reported evidence
supporting the differential mortality hypothesis (i.e.
selection) in seven of 24 (29%) studies. Most empirical
studies were based on cross-sectional comparisons in
which, in many cases, these two groups of hypotheses
were confounded. Increases in competence have been
found to be an important factor in explaining the increase
in reproductive success with age. For instance, some
studies have found experienced breeders to perform
better than inexperienced breeders while controlling
for age, providing support for the breeding experience
hypothesis (Ainley, LeResche & Sladen 1983; Pyle et al.
1991; Forslund & Larsson 1992; Pärt 1995; Dittmann
& Becker 2003). In contrast, other studies did not find
this effect of experience on breeding success (Perdeck &
Cavé 1992; Newton, Marquiss & Moss 1981; Boekelheide
& Ainley 1989; Raleigh & Rendell 2001).
Here, we found evidence suggesting that increases in
competence within individuals most probably caused
the observed increase in breeding performance with
age, at least until reaching middle age. In contrast, we
found no support for the selection hypothesis because
there was no correlation between life span and breeding
performance. These conclusions were not confounded
by between-individual differences in quality, because
we controlled for such effects in the analysis concerning
within-individual changes in breeding success or laying
date with age. Furthermore, we identified two different
mechanisms associated with an increase in competence.
First, male and female barn swallows advance their
arrival date at the breeding grounds as they age until
reaching middle age. The fitness benefits of early arrival
have been documented widely in birds (Forstmeier
2002; Dittmann & Becker 2003), including this species
(Møller et al. 2004). Early-arriving individuals have a
higher probability of mating, start to reproduce earlier
and have higher fecundity than the average individual
(Møller 1994a,b). Arrival date has been shown to be
condition-dependent, with males in prime condition
arriving early at the breeding grounds. Therefore, age-
ing males and females may increase the skills needed to
perform correctly the tasks related to make the long-
distance migratory journey safely between winter
quarters in Africa and the breeding grounds in Europe.
This increase in competence in migratory performance
with age would finally result in both an advance in laying
date and an increase in breeding success because of the
positive relationship between arrival date, laying date
and breeding success (Møller 1994a,b). However, it was
difficult to disentangle the effects of age from those of
arrival and laying dates on annual fecundity in this cor-
relative study. Although the minimal adequate model
retained main and quadratic terms of female age, the main
effect of female age became non-significant (P = 0·10)
when including female and male arrival date and laying
date as three new explanatory variables. This was because
age, arrival dates and laying dates are correlated with
each other, which precludes us from finding an associ-
ation between these variables and annual fecundity on
the predicted direction at the same time.
Secondly, we also reported an increase in com-
petence due to an increase in breeding experience, as
demonstrated by the larger annual fecundity of breeding
pairs that reproduced together for 2 consecutive years,
compared with that of breeding pairs that reproduced
only in 1 year and hence were less experienced. Con-
versely, Saino et al. (2002), studying a population of
barn swallows in Italy, did not find a reproductive
advantage in terms of clutch size, hatching date, fledg-
ing success or offspring phenotype between pairs that
re-mated for 2 consecutive years compared with pairs
that divorced from one year to the next. These results
and those that we have obtained here are not compara-
ble, because in the study by Saino et al. (2002), divorced
pairs were considered to be those in which both members
survived but did not re-mate, while in the present study
less experienced pairs did not re-mate mainly because
one of the pair members died between one breeding
season and the next.
A previous study of age-dependent changes in repro-
ductive traits and senescence in barn swallows has shown
that reproductive success increased in early life, reach-
ing a plateau in middle age and decreasing in old age
(Møller & de Lope 1999). However, that study did not
explore the effect of female and male age on breeding
success separately and therefore could not establish the
independent effect of female and male age on fecundity.
The present study confirmed age-dependent relation-
ships with fecundity and showed that it was due speci-
fically to an age effect of females. Our study was based
on a large sample size, and therefore the power of the
statistical tests was large. Studies considering the age of

923
Breeding
performance in
early and late life
and age
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
915–925
both sexes suggested that performance can vary more
closely with either sex depending on species-specific
reproductive roles of males and females. Examples for
a larger male effect were found in passerines (Nol &
Smith 1987; McCleery et al. 1996; Green 2001), auklets
(Pyle, Sydeman & Hester 2001) and birds of prey (Espie
et al. 2000) and a larger female effect in water-birds
(Forslund & Larsson 1992) and bee-eaters and passerines
(Lessells & Krebs 1989; Desrochers & Magrath 1993;
Smith 1993; Komdeur 1996). In barn swallows, parents
feed the young until a few days after fledging, but females
contribute more to feeding than their mates (Saino
et al. 2002), providing a possible explanation as to why
female age effects were more important than male age
effects in age-dependent fecundity, at least during the
early part of life.
A novel finding of the present study was that female
and male age was related to timing of breeding in barn
swallows. As far as we know, no association between
female and male age and laying date has been shown
previously in this or other species. Interestingly, the age
of males was related to timing of breeding in a similar
way to females. This means that females could benefit
by mating with middle-aged males and males by mating
with middle-aged females, because this will advance the
onset of reproduction of the pair. Therefore, it would be
adaptive for each individual to mate with middle-aged
mates because this is the optimal age for which lying
date was earliest. Future research could focus on indi-
vidual mating preferences with respect to age, with the
aim of trying to disentangle age effects from mating
preferences for phenotype traits (for example, tail
length). Experimental studies could manipulate the
tail length of males and females of different age-classes.
For example, tails of individuals of different age could
be shortened or elongated to an average of middle-aged
individuals, allowing to test for mating preference with
respect to age while controlling for tail length. Mating
preferences for tail length could be tested by manipu-
lating tail length within different age-classes, thereby
controlling for age effects.
Future research might also focus upon testing the
optimization of reproductive effort (restraints hypoth-
esis), which was not evaluated in the present study. This
hypothesis predicts that the relative amount of resources
allocated to reproduction should increase with age. If
survival probability decreases only late in life, as
expected in the barn swallow, reproductive effort should
increase at old age. Observational studies could evalu-
ate investment in reproduction of individuals belonging
to different age-classes, with special focus on old age
classes. Experimental studies, for example, could mani-
pulate brood size for breeding individuals of different
ages. Old individuals should invest more in reproduc-
tion than young individuals, specifically when caring
for an enlarged brood.
Our long-term study allowed us to quantify within-
individual deterioration in two reproductive traits (i.e.
annual fecundity and laying date) and one migratory
trait (i.e. arrival date) late in life, while controlling for
between-individual variation. This finding provides
evidence of the existence of senescence in fecundity and
arrival date, as shown previously (Møller & de Lope 1999),
and in laying date. Linear mixed models revealed con-
siderable variation among individuals in laying date,
annual fecundity and arrival date. Individual differences
in laying date, annual fecundity and female or male
arrival date were not associated with age at last repro-
duction because neither linear nor quadratic terms were
significant in LME. Therefore, the quality of female
breeders with respect to timing of breeding or breeding
success or the quality of male and female with respect
to arrival date was represented equally among the over-
all range of age-classes.
In conclusion, the observed increase in breeding per-
formance with age in early life was related to a within-
individual increase in breeding experience and migratory
performance as individuals aged, providing support
for the ‘constraints hypothesis’. Conversely, we did not
find evidence for the disappearance of poor-quality
individuals among age-classes and, hence, the ‘selection
hypothesis’ was not supported. Fecundity was affected
specifically by age of the breeding female, probably
because females invest more in the late stage of repro-
duction, feeding offspring more extensively than their
mates. The age of the two members of a breeding pair
affected the onset of reproduction in a similar manner,
which could have consequences for the mating prefer-
ences of individuals with respect to age. We confirmed
the existence of senescence in fecundity and arrival date
and found that laying date also deteriorated in late life.
Acknowledgements
We are grateful to all the people that help to obtain data
in the field: F. Mateos, C. Navarro, P. Ninni, J. Cuervo,
A. Barbosa and S. Merino. The study was supported by
the Spanish Ministry of Education and Science (CGL
2006–2913).
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Received 30 January 2007; accepted 30 April 2007