Winter food provisioning reduces future breeding performance in a wild bird

Abstract

Supplementation of food to wild birds occurs on an enormous scale worldwide, and is often cited as an exemplar of beneficial human-wildlife interaction. Recently it has been speculated that winter feeding could have negative consequences for future reproduction, for example by enabling low quality individuals to recruit into breeding populations. However, evidence that winter feeding has deleterious impacts on reproductive success is lacking. Here, in a landscape-scale study of blue tits (Cyanistes caeruleus) across multiple years, we show that winter food supplementation reduced breeding performance the following spring. Compared to unfed populations, winter-fed birds produced offspring that weighed less, were smaller, and had lower survival. This impairment was observed in parents that had received fat only, or in combination with vitamin E, suggesting some generality in the mechanism by which supplementary feeding affected reproduction. Our results highlight the potential for deleterious population-level consequences of winter food supplementation on wild birds.

Full text

Winter food provisioning reduces future
breeding performance in a wild bird
K. E. Plummer
1
*, S. Bearhop
1
, D. I. Leech
2
, D. E. Chamberlain
3
& J. D. Blount
1
1
Centre for Ecology and Conservation, College of Life & Environmental Sciences, University of Exeter, Cornwall Campus, Penryn,
Cornwall, TR10 9EZ, UK,
2
British Trust for Ornithology, The Nunnery, Thetford, Norfolk, IP24 2PU, UK,
3
Dipartimento di Scienze
della Vita e Biologia
`
dei Sistemi, Universita
`
degli Studi di Torino, Via Accademia Albertina 13, 10123 Turin, Italy.
Supplementation of food to wild birds occurs on an enormous scale worldwide, and is often cited as an
exemplar of beneficial human-wildlife interaction. Recently it has been speculated that winter feeding could
have negative consequences for future reproduction, for example by enabling low quality individuals to
recruit into breeding populations. However, evidence that winter feeding has deleterious impacts on
reproductive success is lacking. Here, in a landscape-scale study of blue tits (
Cyanistes caeruleus
) across
multiple years, we show that winter food supplementation reduced breeding performance the following
spring. Compared to unfed populations, winter-fed birds produced offspring that weighed less, were
smaller, and had lower survival. This impairment was observed in parents that had received fat only, or in
combination with vitamin E, suggesting some generality in the mechanism by which supplementary feeding
affected reproduction. Our results highlight the potential for deleterious population-level consequences of
winter food supplementation on wild birds.
V
ariation in food availability has profound effects on individual life-histories and the regulation of popu-
lation dynamics
1
. The supply of food to animal populations is often perturbed through human activities. In
particular, supplementation of food to wild animals is extensively applied as a conservation tool and often
yields almost immediate increases in productivity
2–5
. However, studies of its downstream effects have highlighted
some issues of concern such as biasing of primary sex ratios
6
, and increased disease transmission
7
. In addition to
specific conservation projects, food supplementation to wildlife is in fact practiced on a far larger scale in gardens
and backyards. For those species which use supplementary food in the UK, there is an estimated one feeder for
every nine individual birds
8
, and similar levels of provisioning occur across much of the Western World
9–12
.
Supplementary feeding of birds therefore represents an enormous perturbation of natural resource availability.
Food supplementation is predicted to benefit wild birds
11
, although a range of impacts seems possible. Recently
it has been reported that food supplementation to birds whilst they are breeding can have immediate effects on
diurnal activity patterns
13
and result in reduced reproductive success
14
. However, it is unclear whether similarly
deleterious effects may arise as a consequence of winter food supplementation. This is important because
supplementary feeding is especially common during winter when there is an assumption that wild birds could
benefit from being ‘helped’, yet there is considerable uncertainty about its impacts on future breeding perform-
ance
10,15,16
. Carry-over effects occur where events or life history decisions in one season or year influence events in
a subsequent season or year
15
. Such carry-over effects are thought to be widespread and to have important
consequences for fitness in wild populations of animals, although there have so far been few experimental
demonstrations of their existence
15
. Food supplementation in winter can have almost immediate benefits for
survival (e.g.
17,18
), and consequently it can result in increased recruitment and greater breeding densities the
following spring
19
. However, only a single study to date has considered the effects of winter food supplementation
on future reproductive success: winter feeding of blue tits (Cyanistes caeruleus) enabled birds to breed earlier and
fledge more offspring during the following spring
20
. In contrast, it has been speculated that winter food supple-
mentation could also have deleterious impacts. For example it may result in receipt of an unbalanced diet, or lead
to negative density dependent processes and changes to the phenotypic structure of breeding populations as a
consequence of increased over-winter survival
10,16,21
. Alternatively, food supplementation during winter could
create an ‘ecological trap’ where birds receive inaccurate cues as to future natural food availability, and conse-
quently make unsustainable investments in breeding
16
. If such effects are manifest they would be expected to
cause reduced reproductive success at the population level.
Carry-over effects produced by winter supplementation might be influenced by the nutritional composition of
foods. Items commonly provisioned to wild birds such as nuts, seeds and fats are rich in energy and lipophilic
OPEN
SUBJECT AREAS:
CONSERVATION
ECOPHYSIOLOGY
BEHAVIOURAL ECOLOGY
EVOLUTIONARY ECOLOGY
Received
10 April 2013
Accepted
28 May 2013
Published
20 June 2013
Correspondence and
requests for materials
should be addressed to
J.D.B. (j.d.blount@
exeter.ac.uk) or K.E.P.
(kate.plummer@bto.
org)
* Current address:
British Trust for
Ornithology, The
Nunnery, Thetford,
Norfolk, IP24 2PU, UK.
SCIENTIFIC REPORTS | 3 : 2002 | DOI: 10.1038/srep02002 1

antioxidants such as vitamin E
22,23
. Daily energy acquisition is a key
determinant of winter survival in small passerine species of birds,
which can readily fall into negative energy balance when natural food
is scarce
17,24
. However, over-reliance on supplemental energy-rich
foods such as fats to the detriment of a balanced diet could be harm-
ful
21
. Furthermore, passerine species cannot store energy to any great
extent. Therefore, with the exception of caching species, energy
sequestered from the diet in winter is unlikely to fuel later reproduc-
tion
25
. Lipophilic antioxidants, on the other hand, may enhance
health through effects on immunity and antioxidant defence
22,26
and can be stored in large quantities in body tissues
27,28
. As such, it
has been hypothesised that antioxidants in body storage could influ-
ence reproduction in later seasons or years
29
. In addition, the impacts
of winter food supplementation on wild bird species are likely to be
influenced by stochastic variation in natural food availability
18,30
.To
detect such impacts therefore requires a landscape-scale experi-
mental approach that encompasses multiple sites and years.
Using a three year experimental study conducted across nine
woodland sites, we investigated the impacts of winter supplementa-
tion of energy- and antioxidant-rich foods on future reproduction in
blue tits. Woodland populations of tits were randomly allocated to
receive either fat (n 5 3), fat plus vitamin E (n 5 3), or remained
unfed as a control (n 5 3). The experiment was conducted over three
years (2008–2010), and treatments were rotated amongst sites across
years to control for any site-specific effects on breeding performance.
Using woodland populations allowed greater control of the context
and quantity of food provisioning than could have been achieved
within an urban environment. Since natural food and breeding
resources are anticipated to be more accessible to woodland birds
31
,
our results are predicted to be a conservative estimate of the con-
sequences of winter provisioning within a strictly urban landscape.
Results
There were no significant effects of winter food supplementation on
nest box occupancy (binomial GLMM; n 5 467 out of 1038 boxes
occupied over 3 years x
2
2
5 3.17, P 5 0.21). The timing of laying and
clutch size also did not vary in response to food supplementation, as
previously described in Plummer et al. (2013)
21
. Hatching success
was marginally higher in fat plus vitamin E-fed populations com-
pared to the other treatment groups (Table 1; binomial GLMM; n 5
362, x
2
2
5 5.44, P 5 0.066). However, compared to unfed controls,
parents that had been supplemented in the previous winter produced
offspring that weighed less and were structurally smaller, and as a
Table 1
|
Summaries of breeding parameters (mean 6 s.e.m) by winter feeding treatment and year between 2008–2010
Year
Treatment meanBreeding parameter Treatment 2008 2009 2010
Boxes occupied (%) Unfed 37.7 6 5.9 38.9 6 11.8 47.2 6 8.2 41.3 6 4.7
Fat 41.8 6 6.5 45.7 6 3.7 48.6 6 8.9 45.4 6 3.5
Fat 1 Vit E 43.7 6 14.9 44.3 6 10.7 53.0 6 0.3 47.0 6 5.5
Annual mean 41.1 6 5.1 43.0 6 4.8 49.6 6 3.6
Lay date [1 5 1 April] Unfed 27.6 6 1.2 24.3 6 0.9 29.6 6 0.9 27.3 6 0.6
Fat 26.4 6 1.0 24.6 6 1.0 29.3 6 0.7 26.8 6 0.5
Fat 1 Vit E 26.0 6 1.0 25.4 6 1.0 31.7 6 1.0 28.0 6 0.6
Annual mean 26.6 6 0.6 24.8 6 0.6 30.2 6 0.5
Clutch size Unfed 8.0 6 0.2 8.5 6 0.3 8.3 6 0.2 8.3 6 0.2
Fat 8.0 6 0.3 7.8 6 0.2 8.6 6
0.2 8.2 6 0.1
Fat 1 Vit E 8.5 6 0.3 7.7 6 0.3 7.6 6 0.2 7.9 6 0.1
Annual mean 8.2 6 0.2 8.0 6 0.2 8.2 6 0.1
Hatching success (%) Unfed 91.5 6 2.3 87.2 6 2.6 91.0 6 2.6 89.9 6 1.4
Fat 93.1 6 2.3 91.7 6 2.6 88.0 6 2.7 90.6 6 1.5
Fat 1 Vit E 93.1 6 2.0 90.6 6 2.3 95.1 6 1.5 92.9 6 1.2
Annual mean 92.6 6 1.3 89.9 6 1.4 91.1 6 1.4
8.0
8.5
9.0
9.5
10.0
10.5
unfed fat fat + Vit E
Winter feeding treatment
Chick mass (g)
a
**
**
30
40
50
60
70
80
unfed fat fat + Vit E
Winter feeding treatment
Fledging success (%)
b
***
**
Figure 1
|
Differences in (a) chick mass and (b) fledging success in
response to winter feeding. Mean 6 s.e.m plotted using raw values.
Significance of post-hoc pairwise comparisons shown, where ** 5 P # 0.01
and *** 5 P # 0.001.
www.nature.com/scientificreports
SCIENTIFIC REPORTS | 3 : 2002 | DOI: 10.1038/srep02002 2

consequence fledged an average of 8% fewer offspring (Fig. 1,
Table 2). Indeed, the body mass and head-bill length of chicks 12
days post-hatching strongly predicted their subsequent fledging suc-
cess in all treatments and years (binomial GLMM, n 5 288; brood
mean mass: x
2
1
5 122.97, P , 0.001; brood mean head-bill length: x
2
1
5 70.61, P , 0.001). These deleterious effects were irrespective of the
specific type of food that was supplemented during the previous
winter (Fig. 1, Table 2). Furthermore, there was significant annual
variation in all breeding measures (x
2
$ 8.71, P # 0.013) except nest
box occupancy and hatching success (P $ 0.13). But the effects of
treatment were not significantly influenced by year in any instance
(treatment 3 year interaction: P $ 0.096).
Table 2
|
Effects of winter food supplementation of parents on (a) chick mass, (b) chick head-bill length and (c) fledging success during the
subsequent breeding season
Fixed effect Factor level Estimate 6 s.e.m
x
2
d.f. P
(a) Chick mass
Treatment
a
Fat 21.749 6 1.387 10.83 2 0.004**
Fat 1 Vit E 25.033 6 1.436
Year
b
2009 20.503 6 0.166 9.01 2 0.011*
2010 20.255 6 0.172
Hatching date 20.003 6 0.021 7.83 1 0.005**
Brood size 20.240 6 0.039 35.01 1 ,0.001***
Nestling age 0.436 6 0.093 21.50 1 ,0.001***
Treatment 3 hatch date
a
Fat 0.026 6 0.028 10.52 2 0.005**
Fat 1 Vit E 0.093 6 0.029
(b) Chick head-bill length
Treatment
a
Fat 20.334 6 0.101 12.93 2 0.002**
Fat 1 Vit E 20.307 6 0.103
Year
b
2009 20.550 6 0.105 8.71 2 0.013*
2010 20.245 6 0.109
Hatching date 0.018 6 0.008 4.62 1 0.032*
Brood size 20.093 6 0.023 13.32 1 ,0.001***
Nestling age 0.549 6 0.059 74.52 1 ,0.001***
(c) Fledging success
Treatment
a
Fat 20.599 6 0.188 15.21 2 ,0.001***
Fat 1 Vit E 20.729 6 0.194
Year
b
2009 0.687 6 0.179 14.83 2 ,0.001***
2010 0.452 6 0.194
Hatching date 0.037 6 0.018 4.23 1 0.040*
All main effects and significant interaction terms within each minimum adequate model are reported, following stepwise deletion of non-significant terms.
a
Winter feeding treatment relative to unfed controls.
b
Relative to 2008.
0 1020304050
4
6
8
10
12
14
Provisioning rate (visits per 30 min)
Chick mass (g)
unfed
fat
fat + Vit E
Figure 2
|
Relationship between parental nest visit rate and chick mass. Brood means 6 s.e.m are plotted and lines fitted using parameter estimates
from the minimum adequate model. Post-hoc comparisons showed that the relationship was significantly different for unfed parents compared to
fat-fed (P 5 0.046) and fat plus vitamin E-fed (fat 1 Vit E) parents (P 5 0.017).
www.nature.com/scientificreports
SCIENTIFIC REPORTS | 3 : 2002 | DOI: 10.1038/srep02002 3

We predicted that variation in offspring size and survival could
result from differences in parental brood-rearing capacity carried-
over from the winter feeding treatment. Therefore, we conducted a
concurrent investigation to assess the extent to which variation in
chick mass at day 12 was explained by parental nest visit rates during
the first year of the study. Data were collected using video recordings
at 59 nests across all nine woodlands and all three feeding treatments.
Parental nest visit rates did not differ significantly amongst treat-
ments (Poisson GLMM; n 5 59, x
2
2
5 2.05, P 5 0.36). However, nest
visit rate positively predicted chick mass and this relationship dif-
fered amongst treatments (GLMM; n 5 300, treatment 3 nest visit
rate interaction: x
2
2
5 8.11, P 5 0.017). There was no significant
relationship between nest visit rate and the mass of chicks produced
by unfed (control) parents, which were heavier on average (Fig. 1a).
However, nest visit rate significantly predicted the mass of chicks
produced by winter-fed parents of both food supplementation treat-
ments (Fig. 2). Therefore, whilst winter-fed parents did not exhibit a
reduction in nest visits per se, the quantity and/or nutritional value of
delivered food items was clearly diminished.
Discussion
The results of this study cast doubt on the assumption that supple-
mentary feeding of wild birds is invariably beneficial at the popu-
lation level. Winter food supplementation resulted in reduced
breeding success the following spring, several weeks after the provi-
sioning of food had ended. Our results therefore provide an experi-
mental demonstration of a carry-over effect, one of few such
examples reported in a wild animal
15
. The capacity for within season
food supplementation to influence reproduction in wild birds varies
amongst sites and across years, for example in response to variation
in natural food supply
18,32–35
. Such variance across years is clearly
evident from the results of the present study (see Table 1). Yet,
despite taking into account these notable sources of variation by
conducting our research at nine woodlands and over three years,
the overwhelming pattern which emerged was of deleterious impacts
of winter food supplementation on future breeding performance.
Marginal increases in hatching success following vitamin E pro-
visioning suggest that females were able to improve egg investment to
some extent following increased antioxidant uptake in winter
21,36
.
However, the negative effects of winter food supplementation on
the weight, size and survival of chicks (Fig. 1), and on parental
chick–rearing capacity (Fig. 2), suggests that initial investments
made by fed parents could not be sustained post-hatching.
Although conducted in a woodland environment, the difference in
fledging success we report between fed and unfed populations resem-
bles the level of variation in productivity observed between birds in
urban and non-urban landscapes. Fledging success is on average
15.4% (95% confidence range: 8.9–21.9%) lower in urban compared
to rural habitats for passerine bird species
31
. This difference has been
attributed to the multiple costs associated urban living, including
increased predation, greater disease transmission, fragmented hab-
itat structure, road collision risk and reduced food availability
31
. Our
results support the suggestion that supplementary feeding in urban
gardens may also be a contributory factor
14,31
.
There are at least three possible explanations for our findings.
First, winter feeding could have resulted in an unbalanced diet if
birds heavily utilised supplementary food, and subsequently entered
the breeding season in relatively poor nutritional condition. We are
aware of only two previous studies which have experimentally inves-
tigated the effects of winter food supplementation on any aspect of
future reproductive performance in birds. We recently reported that
winter feeding with fat resulted in the production of eggs with rela-
tively small yolks and reduced levels of carotenoid pigments early in
the laying season, compared to birds supplemented with fat plus
vitamin E or which were unfed
21
. In contrast, Robb et al.
20
reported
that winter feeding with peanuts led to earlier laying and increased
fledging success in woodland populations of blue tits in a single year
of study. One possible explanation for this difference is that the
impacts of food supplementation on reproduction depend on the
specific nutritional profile of foods. For example, sulphur-containing
amino acids are potentially limiting for reproduction in birds,
including tits
37
, although peanuts are a relatively poor source of these
nutrients
38
. Dependency on supplemented fats, on the other hand,
while being an excellent source of energy could result in an unbal-
anced diet with negative consequences for reproduction. We found
that reproduction was impaired in populations that had been provi-
sioned with fat, but also in populations which had received fat
together with vitamin E – a potent antioxidant and immunostimu-
lant
22,26
. Therefore, negative effects of a diet rich in fats might over-
ride any benefits of antioxidant intake, although this possibility
awaits study.
Second, through effects on survival and recruitment, winter food
supplementation could have altered the phenotypic structure of
breeding populations, such that they included increased numbers
of individuals that had relatively low reproductive capacity. Third,
winter food supplementation could have caused an ecological trap by
encouraging birds to make unsustainable investments in reproduc-
tion, at localities which had insufficient natural food availability in
spring
10,16
. However, it is difficult to separate these possible mechan-
isms using breeding parameters at the population level as presented
here. For example, we found no significant effect of winter food
supplementation on nest box occupancy, as might be expected if
breeding population density increased as a result of winter feeding
either through greater survival or attraction to feeders. Although the
abundance and utility of natural nesting sites is unknown and as such
a true measure of breeding density is unavailable. To disentangle
such carry-over effects and better understand the efficacy of bird
feeding these possible mechanisms would ultimately require known
individuals to be followed through winter and spring, which is almost
impossible to do in the wild
39
.
In conclusion, this study has shown for the first time that winter
food supplementation had deleterious consequences for future
fledging success. Nevertheless, despite the evidence presented here,
it would be premature to conclude that supplementary feeding is
inevitably deleterious for wild birds. It would be particularly valuable
to assess whether year-round food supplementation can alleviate
negative effects of season-specific feeding. For example in the US,
Florida scrub-jays living in suburban environments are believed to
gain reproductive benefits due to the abundance and predictability of
anthropogenic food sources
40
. Furthermore, how we judge the effi-
cacy of food supplementation to wild birds must depend in part on
whether impacts are assessed at the level of individuals or popula-
tions. For some individuals, the receipt of supplementary food may
improve their lifetime reproductive success if they would otherwise
have been unable to survive and recruit, or to reach a condition
threshold necessary to breed. However, recruitment of such indivi-
duals might result in reduced mean productivity at the population
level. Whether prolonged winter provisioning could bring about
declines in the population sizes of wild birds in the long-term is an
important question for future study. We note that there is no indica-
tion that overall numbers of blue tits in the UK have declined; in fact
numbers have remained stable since 1995
41
. However, potential rela-
tionships between winter food supplementation and trends in popu-
lation sizes of birds have not been investigated for any species. With
garden bird feeding promoted as a method for conserving declining
wild bird populations, these new insights suggest much more needs
to be done to fully understand its impacts.
Methods
Study sites and experimental design. The study was conducted at nine deciduous
woodlands in Cornwall, UK. Study woodlands averaged 10.7 hectares (61.1 s.e.m)
and were situated at least 2 km apart. The predominant tree species were oak
(Quercus spp.), beech (Fagus sylvatica) and sweet chestnut (Castanea sativa).
www.nature.com/scientificreports
SCIENTIFIC REPORTS | 3 : 2002 | DOI: 10.1038/srep02002 4

Woodlands were grouped into triplets according to their tree, understorey and
ground cover species composition. Within sites, feeders and nest boxes were
positioned at an equal density and distribution of ca. one feeder and four nest boxes
per hectare. Given that woodlands were of a comparable size with nest boxes provided
at equal densities, it is unlikely that our findings were influenced by density-
dependent effects. The winter food supplementation experiment was conducted over
three years from 2007 to 2009 (14 December – 4 March 2007/08; 18 November – 11
March 2008/09 and 2009/10), and potential carry-over effects on reproductive
success were investigated during the subsequent springs, 2008–2010. In the first year
of the study, each site within a triplet was randomly allocated to a feeding treatment:
unfed (control), fat, or fat plus vitamin E. Treatments were rotated within triplets
across years, so that every site received all three treatments over the course of the
study. Therefore the potential confounding effect of variation in site quality was
controlled for in the experimental design.
Winter food supplementation. All feeding stations were provisioned with a new
150 g fat ball every 10 days. Fat balls were produced 1–2 days in advance of
provisioning, using solid vegetabl e fat (Crisp ‘n Dry, Princes Ltd., Liverpool, UK) and
a small amount of yellow food colouring to increase food uptake by birds (0.125 mL
100 g
21
fat; ASDA Natural Food Colouring, Asda Stores Ltd., Leeds). Fat balls for the
fat plus vitamin E treatment group were supplemented with a-tocopherol (T3251;
Sigma-Aldrich, Dorset, UK) at a concentration of 100 mg kg
21
fat, a level equivalent
to that found in peanuts
42
. Lipophilic antioxidants cannot be provisioned to birds
without the use of fat or oil as a ‘carrier’, and such antioxidants are always co-acquired
with lipids in natural foods
43
. All supplements were prepared using standardised
methods
21
, and were predominantly utilised by the target species. Winter misting
netting and stable isotope analysis confirmed the use of winter supplemented food by
breeding birds.
Breeding success parameters. Nest boxes were inspected every 1–3 days from April
to June to determine laying date, clutch size, brood size and fledging numbers.
Hatching success was defined as the proportion of a clutch that hatched, and fledging
success as the proportion of hatchlings that fledged. Morphometric measures were
recorded for all surviving chicks at 12 days post-hatching (61 day; mean chick age 6
s.e.m: 12.19 6 0.02, n 5 1706, brood n 5 319). Body mass (60.1 g) was recorded
using an electronic balance and head – bill length (60.05 mm) measured twice with
dial callipers then averaged
44
.
Parental visit rates. Parental visit rates to nests were recorded on day 11 (61 day; n 5
59) of the nestling phase during the first breeding season (2008). Nest boxes were
filmed for 30 min using a Sony DCR – HC37E Handycam at 0630 GMT or 0830
GMT. Chick age and filming time did not differ significantly between treatment
groups (GLMs: P . 0.15). Parental visit rate, defined as the number of visits per
30 min, was extracted from video playbacks. The sex of parents could not be
distinguished from the video recordings, and therefore nest mean visit rates were
calculated.
Statistical analyses . All statistical analyses were conducted using R version 2.12.2
45
.
Data were analysed using general/generalised mixed effects models (GLMMs) and
backwards stepwise deletions of non-significant terms, with alpha set at 0.05.
Hatching and fledging success data were fitted using binomial errors and parental
nest visit rates using Poisson errors, after checking for overdispersion. Remaining
analyses were completed using a Gaussian error distribution, and the normality and
homoscedasticity of residuals were checked prior to model simplification. For
analysis of nest box occupancy, lay date, clutch size, hatching and fledging success,
nest box identity nested within woodland site was specified as the random term to
control for pseudoreplication. Brood identity was included as a random term, nested
within nest box identity, in analyses of chick phenotypes to control for non-
independence of chicks within broods. Nest box identity was excluded from analyses
involving parental nest visit rate, as boxes were only used once within a given year.
Winter food supplementation treatment, year and lay/hatching date were included as
explanatory variables in all relevant models. Brood size at hatching and chick age at
sampling were additionally controlled for in chick analyses. All two-way interactions
involving treatment were fitted in all models. For post-hoc testing, ANOVA was used
to compare the minimum GLMM model with replicate models in which two
treatment groups under comparison were paired. A total of 467 boxes were nested in
by blue tits over the study period. Lay date analysis included all clutches, but for all
subsequent analyses clutches with laying breaks .2 days (n 5 23) and/or abandoned
prior to incubation (n 5 32) were excluded. Only hatched clutches were considered in
hatching and fledging success analyses (n 5 362). Broods abandoned within one day
of sampling activities, or which could not be regularly monitored due to time
constraints (n 5 28) were excluded from chick size and fledging analyses. These data
filters were not biased amongst treatment groups (P . 0.11).
1. Lack, D. The Natural Regulation of Animal Numbers. (Oxford University Press,
1954).
2. Armstrong, D. P., Castro, I. & Griffiths, R. Using adaptive management to
determine requirements of re-introduced populations: the case of the New
Zealand hihi. J. Appl. Ecol. 44, 953–962 (2007).
3. Oro, D., Margalida, A., Carrete, M., Heredia, R. & Dona
´
zar, J. A. Testing the
goodness of supplementary feeding to enhance population viability in an
endangered vulture. PLoS One 3, e4084 (2008).
4. Schoech, S. J. et al. Food supplementation: A tool to increase reproductive output?
A case study in the threatened Florida Scrub-Jay. Biol. Conserv. 141, 162–173
(2008).
5. Lo
´
pez-Bao, J. V., Palomares, F., Rodrı
´
guez, A. & Delibes, M. Effects of food
supplementation on home-range size, reproductive success, productivity and
recruitment in a small population of Iberian lynx. Anim. Conserv. 13, 35–42
(2009).
6. Clout, M. N., Elliott, G. P. & Robertson, B. C. Effects of supplementary feeding on
the offspring sex ratio of kakapo: a dilemma for the conservation of a polygynous
parrot. Biol. Conserv. 107, 13–18 (2002).
7. Blanco, G., Lemus, J. A. & Garcı
´
a-Montijano, M. When conservation
management becomes contraindicated: impact of food supplementation on
health of endangered wildlife. Ecol. Appl. 21, 2469–2477 (2011).
8. Davies, Z. G. et al. A national scale inventory of resource provision for biodiversity
within domestic gardens. Biol. Conserv. 142, 761–771 (2009).
9. Lepczyk, C. A., Mertig, A. G. & Liu, J. Assessing landowner activities related to
birds across rural-to-urban landscapes. Environ. Manage. 33, 110–125 (2004).
10. Jones, D. N. & Reynolds, S. J. Feeding birds in our towns and cities: a global
research opportunity. J. Avian Biol. 39, 265–271 (2008).
11. Toms, M. P. & Sterry, P. Garden Birds and Wildlife. (AA, 2008).
12. O’Leary, R. & Jones, D. N. The use of supplementary foods by Australian magpies
(
Gymnorhina tibicen): implications for wildlife feeding in suburban
environments. Austral Ecol. 31 , 208–216 (2006).
13. Saggese, K., Korner-Nievergelt, F., Slagsvold, T. & Amrhein, V. Wild bird feeding
delays start of dawn singing in the great tit. Anim. Behav. 81, 361–365 (2011).
14. Harrison, T. et al. Does food supplementation really enhance productivity of
breeding birds? Oecologia 164, 311–320 (2010).
15. Harrison, X. A., Blount, J. D., Inger, R., Norris, D. R. & Bearhop, S. Carry-over
effects as drivers of fitness differences in animals. J. Anim. Ecol. 80, 4–18 (2011).
16. Robb, G. N., McDonald, R. A., Chamberlain, D. E. & Bearhop, S. Food for thought:
supplementary feeding as a driver of ecological change in avian populations.
Front. Ecol. Environ. 6, 476–484 (2008).
17. Brittingham, M. C. & Temple, S. A. Impacts of supplemental feeding on survival
rates of black-capped chickadees. Ecology 69, 581–589 (1988).
18. Kallander, H. The effects of provision of food in winter on a population of the great
tit Parus major and the blue tit P. caeruleus. Ornis Scand. 12, 244–248 (1981).
19. Newton, I. Population limitations in birds. (Academic Press, 1998).
20. Robb, G. N. et al. Winter feeding of birds increases productivity in the subsequent
breeding season. Biol. Lett. 4, 220–223 (2008).
21. Plummer, K. E., Bearhop, S., Leech, D. I., Chamberlain, D. E. & Blount, J. D. Fat
provisioning in winter impairs egg production during the following spring: a
landscape-scale study of blue tits. J. Anim. Ecol., 673–682 (2013).
22. Catoni, C., Peters, A. & Schaefer, H. M. Life history trade-offs are influenced by the
diversity, availability and interactions of dietary antioxidants. Anim. Behav. 76,
1107–1119 (2008).
23. Venkatachalam, M. & Sathe, S. K. Chemical composition of selected edible nut
seeds. J. Agr. Food Chem. 54, 4705–4714 (2006).
24. Koivula, K., Orell, M., Rytkonen, S. & Lahti, K. Fatness, sex and dominance:
seasonal and daily body mass changes in willow tits. J. Avian Biol. 26, 209–216
(1995).
25. Drent, R. H. & Daan, S. The prudent parent - energetic adjustments in avian
breeding. Ardea 68 , 225–252 (1980).
26. Monaghan, P., Metcalfe, N. B. & Torres, R. Oxidative stress as a mediator of life
history trade-offs: mechanisms, measurements and interpretation. Ecol. Lett 12,
75–92 (2009).
27. Surai, P. F. Natural Antioxidants in Avian Nutrition and Reproduction. 2 edn,
(Nottingham University Press, 2007).
28. Negro, J. J., Figuerola, J., Garrido, J. & Green, A. J. Fat stores in birds: an
overlooked sink for carotenoid pigments? Funct. Ecol. 15, 297–303 (2001).
29. Metzger, B. & Bairlein, F. Fat stores in a migratory bird: a reservoir of carotenoid
pigments for times of need? J. Comp. Phys. B 181, 269–275 (2011).
30. Lambrechts, M. M. et al
. Habitat quality as a predictor of spatial variation in blue
tit reproductive performance: a multi-plot analysis in a heterogeneous landscape.
Oecologia 141, 555–561 (2004).
31. Chamberlain, D. E. et al. Avian productivity in urban landscapes: a review and
meta-analysis. Ibis 151, 1–18 (2009).
32. Arnold, T. W., Alisauskas, R. T. & Ankney, C. D. Egg composition of American
coots in relation to habitat, year, laying date, clutch size, and supplemental
feeding. Auk 108, 532–547 (1991).
33. Svensson, E. & Nilsson, J.-A
˚
. Food-supply, territory quality, and reproducti ve
timing in the blue tit (Parus caeruleus). Ecology 76, 1804–1812 (1995).
34. Norris, K. Seasonal-variation in the reproductive success of blue tits - an
experimental-study. J. Anim. Ecol. 62, 287–294 (1993).
35. Nager, R. G., Ruegger, C. & Noordwijk, A. J. V. Nutrient or energy limitation on
egg formation: a feeding experiment in great tits. J. Anim. Ecol. 66, 495–507
(1997).
36. Møller , A. P., Karadas, F. & Mousseau, T. A. Antioxidants in eggs of great tits
Parus major from Chernobyl and hatching success. J. Comp. Phys. B 178, 735–743
(2008).
www.nature.com/scientificreports
SCIENTIFIC REPORTS | 3 : 2002 | DOI: 10.1038/srep02002 5

37. Houston, D., Donnan, D. & Jones, P. Use of labelled methionine to investigate the
contribution of muscle proteins to egg production in zebra finches. J. Comp. Phys.
B 165, 161–164 (1995).
38. Basha, S. M. Deposition pattern of methionine-rich protein in peanuts. J. Agr.
Food Chem. 39, 88–91 (1991).
39. Perrins, C. M. British Tits. (Collins, 1979).
40. Schoech, S. J., Bowman, R. & Reynolds, S. J. Food supplementation and possible
mechanisms underlying early breeding in the Florida Scrub-Jay (Aphelocoma
coerulescens). Horm. Behav. 46, 565–573 (2004).
41. British Trust for Ornithology. GardenBird Watch Annual Results 2011. (British
Trust for Ornithology Press, Thetford, 2011).
42. Chun, J., Lee, J. & Eitenmiller, R. R. Vitamin E and oxidative stability during
storage of raw and dry roasted peanuts packaged under air and vacuum. J. Food
Sci. 70, C292–C297 (2005).
43. Blount, J. D. et al. Carotenoids and egg quality in the lesser black-backed gull Larus
fuscus: a supplemental feeding study of maternal effects. P. Roy. Soc. Lond. B. 269,
29–36 (2002).
44. Redfern, C. P. F. & Clark, J. A. Ringers’ Manual. (BTO, 2001).
45. R: A language and environment for statistical computing. R Foundation for
Statistical Computing, Vienna, Austria (ISBN 3-9 00051-07-0, URL http://
www.R-project.org/, 2011).
Acknowledgements
We thank the many landowners and fieldworkers who made this research possible, A.
Wilson for video analysis of parent provisioning data, and N. Carter for logistical support.
We are grateful to K.J. Gaston, T. Tregenza and the anonymous reviewers for helpful
comments on the manuscript. This work was funded by a Natural Environment Researc h
Council (NERC) CASE studentship (to K.E.P., J.D.B., S.B. and D.E.C.), a Royal Society
Research Fellowship (to J.D.B.), the BTO and Gardman Ltd.
Author contributions
K.E.P., S.B., D.I.L., D.E.C. and J.D.B. designed the research. K.E.P. and J.D.B. wrote the first
draft, and the manuscript was reviewed by all the authors. K.E.P. collected and analysed the
data.
Additional information
Competing financial interests: The authors declare no competing financial interests.
How to cite this article: Plummer, K.E., Bearhop, S., Leech, D.I., Chamberlain, D.E. &
Blount, J.D. Winter food provisioning reduces future breeding performan ce in a wild bird.
Sci. Rep. 3, 2002; DOI:10.1038/srep02002 (2013).
This work is licensed under a Creative Commons Attribution-
NonCommercial-NoDerivs 3.0 Unported license. To view a copy of this license,
visit http://creativecommons.org/licenses/by-nc-nd/3.0
www.nature.com/scientificreports
SCIENTIFIC REPORTS | 3 : 2002 | DOI: 10.1038/srep02002 6