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Supplementary feeding restructures urban
bird communities
Josie A. Galbraith
a,1
, Jacqueline R. Beggs
a
, Darryl N. Jones
b
, and Margaret C. Stanley
a
a
Centre for Biodiversity and Biosecurity, School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand; and
b
Environmental Futures Research Institut e and School of Environment, Griffith University, Nathan, QLD 4111, Australia
Edited by James H. Brown, University of New Mexico, Albuquerque, NM, and approved April 6, 2015 (received for review January 22, 2015)
Food availability is a primary driver of avian population regula-
tion. However, few studies have considered the effects of what is
essentially a massive supplementary feeding experiment: the
practice of wild bird feeding. Bird feeding ha s been posited as
an importan t factor influen cing the structure of bird communities,
especially in urban areas, although experimental evidence to
support this is almost entirely lacking. We carried out an 18-mo
experimental feeding study at 23 residential properties to in-
vestigate the effects of bird feeding on local urban avian assem-
blages. Our feeding regime was based on predominant urban
feeding practices in our region. We used monthly bird surveys to
compare avian community composition, species richness, and the
densities of local species at feeding and nonfeeding properties.
Avian community structure diverged at feeding properties and five
of the commonest garden bird species were affected by the
experimental feeding regime. Introduced birds particularly benefitted,
with dramatic increases observed in the abundances of house
sparrow (Passer domesticus) and spotted dove (Streptopelia chinensis)
in particular. We also found evidence of a negative effect on the abun-
dance of a native insectivore, the grey warbler (Gerygone igata). Al-
most all of the observed changes did not persist once feeding had
ceased. Our study directly demonstrates that the human pastime of
bird feeding substantially contributes to the structure of avian commu-
nity in urban areas, potentially altering the balance between native
andintroducedspecies.
avian ecology
|
community composition
|
garden birds
|
human interactions
|
wildlife feeding
N
umerous factors influence the structure of urban bird as-
semblages, including habitat fragmentation, competition,
and predation (1, 2). One of the most critical factors in the
regulation of all animal populations is food resource availability
(3–5). Urban birds have access to novel food resources derived
from human activities. This provisioning may be unintentional,
for example, the foraging of waste or refuse (6), or deliberate in
the form of bird feeding by the public (7). The deliberate act of
feeding birds is common in many parts of the world, including
the United States, United Kingdom, Australia, and New Zealand
(8–12). Large quantities of food, and hence energy and nutrients,
are added into urban systems each year, with birds the primary
target; it is estimated that in 2002 over 450 million kg of seed was
fed to wild birds in the United States alone (13). For species
capable of exploiting these anthropogenic food sources there
may be profound effects on almost every aspect of their ecology
(14, 15). Direct benefits for feeder-visiting birds may include
reduced time foraging or improved body condition, which in turn
may increase reproductive success or survival and lead to pop-
ulation level changes (16–18). A greater availability of food may
artificially inflate the carrying capacity of the urban environment,
resulting in higher densities of species capable of exploiting an-
thropogenic food resources (15, 19).
Very few studies have experimentally investigated the effects
of feeding birds in the urban environment (15), although there is
correlational evidence that this human pastime has a significant
influence on the urban bird community (e.g., refs. 10, 20, and 21).
In the context of enhancing biodiversity of our cities, bird feeding
may, at first glance, be construed as a positive activity by increasing
the capacity of urban areas to support birds (22). However, the
reality is far more complex (17). Biodiversity may be reduced
where a subset of species become dominant at feeding locales,
either through competitive advantage or numerical dominance.
Alternatively, there may be negative effects for the individuals
exploiting supplementary food sources because of, for example,
increased disease transmission (23, 24) and malnutrition (25),
which may lead to reductions in overall population size.
The interpretation of these potential effects differs further
depending on whether the species is native or introduced. En-
hancing carrying capacity of urban areas, for example, would be
unfavorable ecologically where introduced species were likely to
benefit disproportionately. This is a possible scenario in New
Zealand, where urban habitats are characterized by a high pro-
portion of introduced species (26). The most popular food types
provided by the bird-feeding public in New Zealand, bread and
seed (11), are likely to be consumed primarily by introduced
birds rather than natives, as a result of a fundamental partition in
dietary guilds in urban bird assemblages. Native species persist-
ing in urban areas are principally nectarivorous (e.g., t
u
ı Prosthe-
madera novaeseelandiae), insectivorous (e.g., grey warbler Gerygone
igata), or frugivourous (e.g., New Zealand pigeon Hemiphaga
novaeseelandiae), compared with the typically granivorous or
omnivorous introduced species (e.g., house sparrow Passer
domesticus and common myna Acridotheres tristis, respectively)
(27, 28). Consequently, common feeding practices in New Zea-
land may be supporting increased densities of introduced birds in
urban areas.
In this study we sought to test the hypothesis that supple-
mentary feeding restructures local bird communities, by using an
experimental in situ approach. We established a series of feeding
stations (n = 11) in volunteers’ gardens in urban Auckland, New
Zealand (Fig. 1). These were active for 18 mo, with a feeding
regime designed to mimic common feeding practices of the
Significance
Bird feeding is essentially a massive global supplementary feed-
ing experiment, yet few studies have attempted to explore its
ecological effects. In this study we use an in situ experimental
approach to investigate the impacts of bird feeding on the struc-
ture of local bird assemblages. We present vital evidence that bird
feeding contributes to the bird community patterns we observe in
urban areas. In particular, the study demonstrates that common
feeding practices can encourage higher densities of introduced
birds, with potential negative consequences for native birds.
Author contributions: J.A.G., J.R.B., D.N.J., and M.C.S. designed research; J.A.G. performed
research; J.A.G. analyzed data; and J.A.G., J.R.B., D.N.J., and M.C.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
1
To whom correspondence should be addressed. Email: jgal026@aucklanduni.ac.nz.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1501489112/-/DCSupplemental.
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general public (bread and seed fed daily), ascertained by a nationwide
survey (11). This approach ensured that our results were relevant
and applicable to the current food provisioning in urban areas. We
compared the bird communities at feeding properties with those
at nonfeeding properties (n = 12) before, during, and after the
implementation of the feeding regime. Our main research ques-
tion was: Do typical feeding practices influence the avian species
assemblages observed in urban habitats? Our objectives were to
determine whether feeding had an effect on avian community
composition, species richness, and the densities of local species.
Specifically, we were interested in how typical feeding practices
affect native vs. introduced species, and what happens to local
bird communities once feeding stops. Given the dietary divide
between native and introduced birds in urban New Zealand, we
predicted that typical grain-based feeding practices would in-
crease densities of introduced species.
Results
Initial Observations. Householders in the experimental feeding
group reported that there were dramatic increases of birds at
their properties within weeks of the feeding regime starting. The
time lag for recruitment to the food varied between properties; a
few householders had feeder visitors within a few days, whereas
at one property avian visitors took 2 wk to arrive. Nonetheless,
within approximately 4 wk all feeding stations were well estab-
lished, with feeder visitors coming daily and pre-empting the
provision of food. Once esta blished, birds q uickly removed
the supplementary food at the stations, typically within 2 h of the
food being put out.
Avian Community Composition. A total of 33 bird species (18,228
individuals) were recorded at the study properties, and over 597
bird surveys (10-min point counts), 16 of which were native
species and 17 introduced. Twenty-seven species were recorded
at feeding properties and 31 at nonfeeding properties. The house
sparrow was the most commonly observed species (96.6% of
surveys), followed by blackbird (Turdus merula; 91.1% of surveys),
silvereye (Zosterops lateralis; 90.8% of surveys), and common myna
(87.6% of surveys) ( Table S1). Nonmetric multidimensional
scaling (NMDS) ordination plots indicated that before the start of
the feeding regime avian community composition did not differ
between the two experimental treatment groups (feeding and
nonfeeding properties) (Fig. 2A); this was supported by permuta-
tional multivariate analysis of variance (PERMANOVA) (Table 1)
and permutational analysis of multivariate dispersions (PERMDISP;
F = 0.122, df = 1, P = 0.71). The greatest amount of variation in
community composition before feeding was explained by property
ID and vegetation (R
2
= 0.28 and 0.17, respectively). During ex-
perimental feeding, however, there was evidence of a divergence in
avian communities at feeding compared with nonfeeding properties,
with the feeding-group centroid shifting to the right (Fig. 2B).
PERMANOVA analyses confirmed that provision of food had a
significant effect on community composition (Table 1) and explained
the greatest amount of variation in the data (R
2
= 0.16). The effect
of feeding did vary among months but the proportion of variation
explained by the interaction term was comparatively small (R
2
=
0.04). The proportion of variation explained by property ID and
vegetation were smaller than in the “before” period (R
2
= 0.13 and
0.07, respectively). PERMDISP analyses indicated that that avian
communities were also significantly less variable at feeding
compared with n onfeeding properties in the “feeding ” period
(PERMDISP; F = 35.5, df = 1, P < 0.001). Introduced species
were associated with the community shift at feeding properties,
most distinctly house sparrow and spotted dove (Streptopelia
Fig. 1. Map of northern Auckland, New Zealand, showing the location of properties participating in an experimental bird feeding study. The urban–rural
boundary is also shown, with land zoned as urban shaded in gray. Reference coordinates are expressed as latitude and longitude (WGS84).
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ECOLOGY PNAS PLUS
chinensis)(Fig.2D ). These changes did not persist when the
provision of food stopped (Fig. 2C and Table 1) (PERMDISP; F =
1.03, df = 1, P = 0.34).
Species Richness and Abundance. The mean number of introduced
species recorded per count was well above that for native species
over all properties for the duration of the study (Fig. 3A). We
found no evidence of the onset of the feeding regime having an
effect on species richness overall [see Table S2 for full general-
ized linear mixed model (GLMM) results], instead finding that
feeding had differing effects on introduced and native species
richness (Table 2). Introduced species richness was slightly lower
at feeding compared with nonfeeding properties before the start
of the feeding regime (modeled mean count = 4.25 vs. 4.96 spp.;
Fig. 2. NMDS ordinations of avian community composition (A) before, (B) during, and ( C) after the experimental feeding regime at urban study properties in
northern Auckland, New Zeala nd, grouped by experimental treatment. The dotted ellipses denote the 95% confidence intervals for each experimental (Exp.)
group. The species centroids (relationships among species as defined by their relative abundance at different sites) are also presented (D) for the “during
feeding” period, scaled by percentage of total abundance (square root-transformed) for that period. Species abbreviations (for scientific names see Table S1):
BBGL, southern black-backed gull; BLKB, Eurasian blackbird; CHFN, chaffinch; FNTL, New Zealand fantail; GDFN, goldfinch; GRFN, greenfinch; KNGF, New
Zealand kingfisher; MYNA, common myna; RSLA, eastern rosella; SEYE, silvereye; SPDV, spotted dove; SPRW, house sparrow; STRL, common starling; SWAL,
welcome swallow; THSH, song thrush; TUI, t
u
ı; WBLR, grey warbler.
Table 1. Summary of PERMANOVA results for the effects of feeding treatment (experimental group) on
avian community structure for each experimental period: before, during, and after feeding regime
implementation
Factor
Before During After
df FR
2
P df FR
2
P df FR
2
P
Experimental group 1 3.05 0.021 0.41 1 113.48 0.162 <0.001 1 0.77 0.005 0.67
Month no. 3 1.27 0.027 0.24 17 2.72 0.066 <0.001 3 0.74 0.015 0.79
Vegetation 2 12.10 0.170 0.41 2 24.86 0.071 <0.001 2 12.70 0.167 0.67
Background feeding 2 2.73 0.038 0.41 2 10.90 0.031 <0.001 2 4.82 0.064 0.67
Property ID 17 2.36 0.282 0.41 17 5.20 0.126 <0.001 17 2.79 0.314 0.67
Experimental group × month 3 0.83 0.018 0.63 17 1.52 0.037 <0.001 3 1.04 0.021 0.46
Residuals 63 0.443 356 0.501 63 0.415
Total 91 412 91
F-values (pseudo-F) are derived from 999 permutations. Values in bold are significant at P < 0.05.
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t = −2.39, df = 567, P = 0.03). The introduced species richness of
both experimental groups increased during the feeding period,
but the increase was significantly greater (by 0.66 species) at
feeding properties (Table 2). There was no significant change
from during feeding to after feeding in either group (feeding: t =
0.15, df = 567, P = 0.88; nonfeeding: t = −0.26, df = 567, P = 0.79).
Native species richness was equivalent at feeding and nonfeeding
properties before the start of the feeding regime (modeled mean
count = 2.50 and 2.31 spp., respectively; t = 0.65, df = 567, P =
0.52). At nonfeeding properties, native species richness increased
from before to during the feeding regime (t = 2.61, df = 567, P =
0.009), yet richness at feeding properties did not change (t = −0.25,
df = 567, P = 0.80); this difference in observed pattern was sig-
nificant (Table 2). Native species richness did not change signifi-
cantly in either group after feeding was stopped (feeding: t = −0.22,
df = 567, P = 0.82; nonfeeding: t = 0.90, df = 567, P = 0.37).
There was strong evidence of the feeding regime having an
effect on overall avian abundance (Fig. 3B and Table 2). Before
the feeding regime there was no significant difference in overall
abundance recorded at feeding and nonfeeding properties (mod-
eled mean count = 21.01 and 22.86, respectively; t = −0.97, df =
567, P = 0.33). Both experimental groups showed an increase in
overall abundance from the before period to the during period,
but the increase was significantly more at feeding properties
compared with the nonfeeding properties (modeled mean count
for feeding period = 40.14 vs. 25.95) (Table 2). The pattern of
change from during to after feeding differed significantly be-
tween the two groups (Table 2), with abundance decreasing at
feeding properties (t
= 7.58, df = 567, P < 0.0001) and increasing
at nonfeeding properties (t = −2.39, df = 567, P = 0.02).
Individual Species Responses. We retained the 12 most frequently
observed species for GLMM analyses of individual species re-
sponses to the feeding regime (see Table S2 for full model re-
sults). Among the introduced species there was support for the
feeding regime having an effect on the relative abundance of
four of the eight species analyzed (Table 2). The greatest abso-
lute change in abundance was observed in the most common
species, the house sparrow (Fig. 4A and Table 3). Both feeding
and nonfeeding properties had a significant increase in sparrow
abundance from before to during the feeding regime (t = 11.15,
df = 567, P < 0.0001; t = 2.62, df = 567, P = 0.009, respectively)
but feeding properties had a significantly larger increase (Table 2).
Mean abundance of house sparrow at feeding properties in-
creased from 6.26 before the start of the feeding regime to 19.23
during feeding (Table 3). Sparrow abundance during the feeding
regime was 2.4-times higher at feeding compared with nonfeeding
properties (Table 3). At feeding properties there was a significant
decrease in abundance from the during period to the after period
(t = 9.13, df = 567, P < 0.0001), whereas nonfeeding properties
had a significant increase in abundance (t = −2.61, df = 567, P =
0.009); this difference in pattern was significant (Table 2).
We found a similar effect for spotted dove (Fig. 4E and Table
2), with an obvious increase in abundance at feeding properties
(t = 7.04, df = 567, P < 0.0001) but a decrease in abundance at
nonfeeding properties (t = 3.01, df = 567, P = 0.003) from the
before period to the during period, resulting in 3.6-times more
doves at feeding properties during the feeding regime (Table 3).
There was a significant decrease in the abundance of doves at
feeding properties after feeding had stopped (t = 7.05, df = 567,
P < 0.0001) but no change at nonfeeding properties (t = 0.02,
df = 567, P = 0.98); this difference in the pattern of change was
highly significant (Table 2).
There was also evidence of the feeding regime affecting Eu-
ropean starling (Sturnus vulgaris) and song thrush (Turdus phil-
omelos) abundances (Table 2). A significant increase was seen in
European starling abundance from before to during feeding at
feeding properties (0.35 vs. 0.83 mean individuals per count; t =
3.15, df = 567, P = 0.002) but no change at nonfeeding properties
(t = 0.95, df = 567, P = 0.35). For song thrush, we only detected
an interaction effect from during to after the feeding regime
(Table 2), with abundance decreasing at nonfeeding properties
(t = 2.31, df = 567, P = 0.02) and no significant change for feeding
properties (t = −0.27, df = 567, P = 0.79) (Table 3). Song thrush
abundances did not differ between experimental groups before the
feeding regime (Table 3), but did differ significantly during feed-
ing, with higher abundances at nonfeeding properties (Table 3).
Among the four common native species, there was only evi-
dence of a feeding regime impact on one, the grey warbler, which
significantly decreased in abundance at feeding properties from
0.66 mean individuals per count before feeding to 0.29 during
feeding (t = −3.43, df = 567, P = 0.0007), whereas there was
no significant change at nonfeeding properties (t = 0.04, df =
567, P = 0.96) (Table 2).
Discussion
Changes to Avian Community Structure. Most of our knowledge on
the impacts of feeding wild birds in urban areas derives from
correlational studies or studies conducted in natural habitats
(15). This study directly demonstrates that the pastime of bird
feeding substantially contributes to the avian community pat-
terns observed in urban areas. We found significant changes in
community composition occurring as a result of feeding and
evidence that five common garden bird species were affected by
the experimental feeding regime, despite our study being carried
out on a relatively small scale [11 experimental feeding stations
compared with the estimated 265,000 households feeding birds
across six New Zealand cities (11)]. Our findings support evi-
dence from a number of correlational studies that have found
Fig. 3. Overall (A) species richness and (B) relative abundance of garden
birds recorded during 10-min point counts at urban study properties in north-
ern Auckland, New Zealand, before, during, and after the implementation of
an experimental feeding regime. Experimental (Exp.) group: F, feeding prop-
erties; NF, nonfeeding properties. The vertical dotted lines indicate the start
and end of the feeding regime. Error bars represent the SEM.
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an association between bird feeding and increased densities of
feeding birds in urban areas (e.g., refs. 10, 20, and 21). From
surveying feeding practices we know that ∼two of five house-
holds in New Zealand’s urban areas feed birds (11). Given this
high rate of bird feeding participation, in combination with the
readily observable changes to local bird communities observed in
our study (based on typical feeding practices of the public), we
think it likely the effects of feeding will be operating on a larger
scale as well. Although we need to be cautious of making gen-
eralizations as to the overall effects of feeding on larger spatial
scales, we predict that feeding has important implications for
urban avifaunal assemblages.
Effects on Introduced Birds. Enhancing the capacity of urban en-
vironments to support more species is now a growing area of
research (22, 29, 30); however, not all species are equally de-
sirable. Many of the avian species that have successfully managed
to exploit urban areas are invasive or considered pests (31), such
as the rock pigeon (Columba livia) (22). Identifying what pro-
motes the success of introduced or pest species in these areas is
crucial for developing strategies to enhance native biodiversity
instead. Many introduced bird species in urban areas around the
world are granivores or omnivores, which is ideal for capitalizing
on supplementary food resources. In most countries, though,
there are also native granivores and omnivores present (32, 33)—
usually the primary targets of feeding—with which i ntroduced
species must compete.
Our results support the hypothesis that typical feeding prac-
tices encourage increased densities of introduced bird species in
New Zealand, with obvious and substantial increases in the relative
Table 2. Summary of the effects of the feeding regime on community structure measures and individual species abundances at urban
study properties in northern Auckland, New Zealand
Species/measure
Evidence of feeding
regime effect
Comparison of pattern
between experimental
periods (between feeding
and nonfeeding groups)
Ratio of multiplicative
factors* (F/NF) tP
Overall community structure responses
Overall species richness No During/before 0.21
†
0.58 0.56
During/after −0.10
†
−0.28 0.78
Introduced species richness Yes During/before 0.66
†
2.42 0.015
During/after 0.09
†
0.32 0.75
Native species richness Yes During/before −0.45
†
−2.07 0.039
During/after −0.19
†
−0.86 0.39
Overall abundance Yes During/before 1.68 7.42 <0.0001
During/after 1.69 7.80 <0.0001
Individual responses: Introduced species
House sparrow (Passer domesticus) Yes During/before 2.36 6.10 <0.0001
During/after 2.93 9.13 <0.0001
Common myna (Acridotheres tristis) No During/before 1.72
†
1.36 0.18
During/after 1.23
†
0.52 0.60
Eurasian blackbird (Turdus merula) No During/before 1.33 1.81 0.07
During/after 1.16 1.27 0.20
Spotted dove (Streptopelia chinensis) Yes During/before 6.61 7.52 <0.0001
During/after 3.44 5.24 <0.0001
European starling (Sturnus vulgaris) Yes During/before 1.96 2.04 0.042
During/after 1.09 0.35 0.72
Song thrush (Turdus philomelos)YesDuring/before 0.80 −0.58 0.56
During/after 0.58 −1.98 0.049
Eastern rosella (Platycercus eximius) No During/before 0.71 −0.66 0.51
During/after 0.94 −0.17 0.86
Chaffinch (Fringilla coelebs) No During/before 0.23 −1.18 0.24
During/after 1.01 0.01 0.99
Individual responses: Native species
Silvereye (Zosterops lateralis) No During/before 1.17 0.86 0.39
During/after 1.10 0.51 0.61
T
u
ı (Prosthemadera novaeseelandiae) No During/before 0.82 −0.93 0.35
During/after 1.03 0.14 0.89
Grey warbler (Gerygone igata) Yes During/before 0.43 −2.54 0.011
During/after 0.90 −0.31 0.76
New Zealand fantail (Rhipidura fuliginosa) No During/before 0.75 −0.49 0.62
During/after 0.61 −0.88 0.38
Significance tests for the relevant interaction terms (experimental group × experimental period) from GLMM results are presented, assessing whether
patterns of change between experimental periods (before, during, or after the feeding regime) differ between experimental groups (feeding or nonfeeding).
The ratio of multiplicative factors is the change from one period to the next in the feeding group compared with the nonfeeding group. Significant effects
are highlighted in boldface. Species are listed by mean overall abundance (highest first).
*A ratio of 1 indicates that the change from one period to the next was the same for both the feeding and the nonfeeding groups. A ratio of 2 indicates that
change from one period to the next was two times higher in the feeding group. A ratio of 0.5 indicates that change from one period to the next was 0.5× that
of the nonfeeding group.
†
These measures are interpreted in terms of a difference in the difference in means (period 1 – period 2; feeding – nonfeeding), rather than a ratio of
multiplicative factors, as these measures were modeled using a normal distribution.
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abundance of two species in particular, the house sparrow and
spotted dove, and additional evidence of a positive effect on Eu-
ropean starling. Furthermore, bird communities at feeding prop-
erties exhibited reduced variability and a shift toward communities
dominated by these introduced species. The observed, rapid
changes to house sparrow and spotted dove abundance occurred
after the Austral breeding season, indicating that the effects, at
least initially, were the product of increased juvenile survivorship
and immigration of existing adults from surrounding areas, rather
than an increase in reproductive success. The experimental feeding
regime did encompass one breeding season; therefore, increased
productivity may have contributed to the consistently higher
abundances of these species for the duration of supplementary
feeding (17). However, our data do not allow for this hypothesis
to be tested here; it would require a multiyear study to account
for interannual variation (34). Productivity certainly can be in-
creased with food supplementation, including earlier laying
dates, increased clutch size, and greater hatching and fledging
success (15, 17), although this is not always the case (e.g., ref. 35).
Regardless of the mechanism of increase, the results imply
that feeding promotes a higher carrying capacity for these spe-
cies. House sparrows are already widespread in New Zealand,
whereas spotted doves are more recent invaders and are cur-
rently in the process of expansion, radiating from Auckland City
where they were first introduced in the 1920s (27, 36, 37). We
propose that common feeding practices are aiding this spread, by
supplementing food resources for the doves as they move into
new areas and via increased pressure to disperse from areas of
higher dove density, where they are already established. Feeding
has been linked to range expansions of birds elsewhere, including
Fig. 4. Relative abundance of the 12 (A–L) most commonly occurring garden bird species recorded during 10-min point counts at urban study properties in
northern Auckland, New Zealand, before, during, and after the implementation of an experimental feeding regime. Experimental (Exp.) group: F, feeding
properties; NF, nonfeeding properties. Within each species type (introduced/native) species are listed in order of mean abundance over all counts (n = 597).
For species scientific names see Table 2. The vertical dotted lines ind icate the start and end of the feeding regime. NB: y axis scale varies w ith species.
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native species moving outside of their historical ranges. For ex-
ample, it has been proposed that the northward spread of the
northern cardinal (Cardinalis cardinalis) and American goldfinch
(Carduelis tristis) are linked to the rapid increase in bird feeding
participation in the United States since the 1970s (17).
The effect of the feeding regime on song thrush abundance is
not as conspicuous in comparison with the changes for the house
sparrow or spotted dove. During the feeding regime, song thrush
abundance was generally lower at feeding properties than at non-
feeding properties. We observed a greater decrease in abundance
after the feeding regime ended at nonfeeding properties, likely
because of the already lower abundance at feeding properties.
These results suggest that the feeding regime had a negative ef-
fect on song thrush abundance, perhaps facilitated by the wary
behavior typically exhibited by the species (38) and disturbance by
dominant heterospecifics.
Contrary to our expectation, we did not see an effect of the
feeding regime on common myna (henceforth myna), a key in-
vasive species in New Zealand and globally (28, 39). A number of
factors may have contributed to this result. Interspecific interactions
at feeding stations may have prevented mynas from accessing sup-
plementary food. We observed that mynas were being attracted to
feeding stations, but where stations were congested with other
species—particularly spotted dove—mynas were reluctant to “push
in” to access the food. Therefore, mynas may have been behav-
iorally excluded by dominant heterospecifics when feeders were
busy (40), a scenario likely compounded by the mode of food pre-
sentation. We used a seed feeder and mesh tube to dispense food,
which limits access much more than simply throwing the food on
the ground (the most common method of food presentation) (11),
requiring individuals to contend with others. In addition, the foods
we tested in this study may not have been attractive enough to
encourage higher densities of mynas. Although myna are omni-
vores and will consume the food types we tested, other food types
are more attractive to them, for example dog and cat food, which
is provided by some bird-feeding participants (8, 11). Alternatively,
Table 3. Modeled mean counts of species abundances for the 12 most common garden bird species recorded during 10-min point
counts conducted at urban study properties in northern Auckland, New Zealand
Species Experimental period
Modeled mean
count
Multiplicative factor
(F/NF group) 95% Confidence interval tPNF F
Introduced species
House sparrow Before 6.25 6.26 1.00 (0.71, 1.41) 0.00 0.99
During 8.16 19.23 2.36 (1.85, 2.99) −7.46 <0.0001
After 10.34 8.31 0.80 (0.59, 1.10) 1.47 0.16
Common myna Before 3.89 3.58 −0.31 (-1.23, 0.61) −0.71 0.49
During 2.82 3.05 0.23 (-0.40, 0.87) 0.76 0.46
After 3.17 3.19 0.02 (-0.90, 0.94) 0.05 0.96
Eurasian blackbird Before 1.73 1.35 0.78 (0.55, 1.11) 1.47 0.16
During 2.34 2.43 1.04 (0.85, 1.27) 0.39 0.70
After 2.99 2.68 0.90 (0.68, 1.18) 0.84 0.41
Spotted dove Before 1.32 0.72 0.54 (0.26, 1.14) −1.72 0.10
During 0.80 2.86 3.59 (2.01, 6.43) 4.59 <0.001
After 0.79 0.83 1.05 (0.51, 2.13) 0.13 0.90
European starling Before 1.00 0.35 0.35 (0.16, 0.74) −2.91 <0.01
During 1.21 0.83 0.68 (0.43, 1.08) −1.73 0.10
After 1.69 1.06 0.63 (0.34, 1.15) −1.61 0.13
Song thrush Before 0.42 0.33 0.78 (0.36, 1.72) −0.65 0.53
During 1.02 0.64 0.62 (0.48, 0.81) −3.73 0.002
After 0.63 0.68 1.07 (0.63, 1.80) 0.27 0.79
Eastern rosella Before 0.48 0.64 1.33 (0.38, 4.61) 0.47 0.64
During 0.47 0.44 0.94 (0.43, 2.04) −0.17 0.87
After 0.65 0.65 1.00 (0.38, 2.68) 0.00 0.99
Chaffinch Before 0.03 0.09 3.50 (0.26, 4.70) 1.01 0.33
During 0.24 0.19 0.80 (0.43, 1.49) −0.75 0.46
After 0.30 0.24 0.80 (0.31, 2.07) −0.50 0.62
Native species
Silvereye Before 3.57 3.81 1.07 (0.72, 1.59) 0.34 0.74
During 3.59 4.49 1.25 (1.01, 1.57) 2.03 0.06
After 3.77 4.30 1.14 (0.60, 1.29) −0.71 0.48
T
u
ı Before 1.11 1.34 1.21 (0.60, 2.43) 0.56 0.58
During 1.46 1.44 0.99 (0.55, 1.78) −0.05 0.96
After 1.74 1.67 0.96 (0.49, 1.88) −0.13 0.90
Grey warbler Before 0.35 0.66 1.86 (0.82, 4.25) 1.57 0.13
During 0.36 0.29 0.80 (0.42, 1.51) −0.74 0.47
After 0.31 0.27 0.89 (0.38, 2.08) 0.30 0.77
New Zealand fantail Before 0.12 0.11 1.04 (0.28, 3.82) 0.06 0.95
During 0.34 0.25 1.39 (0.74, 2.60) 1.10 0.29
After 0.14 0.17 0.84 (0.24, 2.93) −0.28 0.78
Species are listed by abundance (highest first). Modeled means control for levels of background feeding and vegetation as well as season, as derived from
GLMMs testing the effect of an experimental feeding regime. Figures are given for each experimental period (before, during, or after the feeding regime),
along with tests of significance between nonfeeding (NF) and feeding (F) groups (from GLMMs). Species are listed by mean overall abundance (highest first).
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www.pnas.org/cgi/doi/10.1073/pnas.1501489112 Galbraith et al.
no effect was found because changes in myna densities were too
transient to be detected; that is, myna numbers increased at
feeding time only with mynas leaving the area immediately after
the food was gone, whereas the survey period encompassed a
longer time period. Other species for which we did not detect an
effect of the feeding regime may also have shown transient changes
at feeding time. However, finding no evidence of an effect es-
sentially means that the feeding regime we implemented was not
capable of influencing the density of those species beyond the
feeding interval.
Effects on Native Birds. We found evidence of the feeding regime
negatively affecting native biodiversity, with native species rich-
ness remaining lower at feeding properties during the feeding
regime compared with before, whereas an increase was observed
at nonfeeding properties. It is arguable, though, whether the
effect detected is biologically significant, given that the differ-
ence in species richness was less than 0.5 species. We suggest its
significance is dependent on scale; at a landscape or regional
scale this effect may well be important when multiple avian as-
semblages are accounted for (41, 42). An important and biolog-
ically significant finding was a decline in grey warbler abundance by
more than 50% at feeding properties during the feeding regime, in
comparison with nonfeeding properties where grey warbler abun-
dance remained steady. This effect is concerning in light of evi-
dence that the grey warbler, regarded as a common species, may in
fact be declining in forest habitats (43). A likely reason for the
negative impact of the feeding regime on warblers is the increased
disturbance by heterospecifics. The grey warbler typically forages
alone or in pairs, gleaning invertebrates from foliage in the sub-
canopy to canopy (27). With densities of other species increasing
dramatically in feeding gardens, the ability of the grey warbler to
forage efficiently would be severely disrupted, especially with, for
example, 50 sparrows occupying a garden on a daily basis, poten-
tially causing displacement (44). In contrast, we did not observe
any negative effects of the feeding regime on another common
insectivore, the New Zealand fantail (Rhipidura fuliginosa); it is
possible that their different behavioral tactics in foraging (primarily
sallying and flush-pursuit) and their tendency to favor associations
with other species when foraging to exploit disturbance (45) allows
for flexibility or resilience where heterospecific densities increase.
Other Impacts. There are a number of other potential conse-
quences of our findings that directly relate to having increased
densities of birds in the urban, or in fact any, environment. As
with the grey warbler, high densities of one or a few dominant
species can affect others through behavioral disturbance or dis-
placement. Aggressive encounters can increase within or between
species, related to higher densities, reduced territory size, or more
time available for such behaviors (46–48). There may also be di-
rect competition for other resources in the area (e.g., other food
sources, nest sites, territory), which in extreme cases could lead to
competitive exclusion and local extinctions (41, 44). Furthermore,
a major issue associated with high bird concentrations is the in-
creased likelihood of transmitting avian diseases (24, 49) and the
associated zoonotic risks to people (50, 51). In addition, there are
potential indirect effects, such as greater predation pressure on
invertebrate populations. A study conducted in Michigan, United
States, found that bird feeding can create areas of concentrated
foraging, with experimentally placed mealworms depredated at
higher rates in the presence of bird feeders (52). Not only would
this affect the invertebrate prey population, but any taxa that are
part of their food web. These findings suggest that the impacts of
common feeding practices in New Zealand could extend beyond
birds, with flow-on effects for other trophic levels.
After Feeding. An important question to address in assessing the
impacts of bird feeding is what happens to bird communities
should feeding stop? In this study we found that most of the
changes to local avian communities associated with feeding did
not persist afterward. The rapid declines in the abundances of
house sparrow and spotted dove once feeding ceased are almost
certainly the result of existing individuals redistributing in the
landscape. It is doubtful that the declines represent mortality
because of dependence on supplementary food, as several studies
have failed to establish dependence as a problem for feeder-vis-
iting birds (13, 53). It is likely that the timeframe of our feeding
regime (18 mo) was too short for more permanent community
changes to occur. Effects, such as competitive exclusion, operate
over much longer timeframes, possibly taking decades to become
apparent (39), or may only be apparent over much larger spatial
scales (41) or when environmentally stressful events occur. Simi-
larly, population changes resulting from altered reproductive
success may only be observable over multiple breeding seasons. As
a consequence we cannot exclude the possibility that reversing the
effects of feeding requires more than purely stopping the provision
of food. This reinforces the need for and the value of long-term
studies of bird-feeding impacts.
Conclusions
The findings of this study are an important step toward under-
standing the impacts of what is essentially one of the largest
wildlife management activities in temperate regions (52). There
are few studies that have experimentally investigated bird feed-
ing, especially in an urban setting (15), perhaps because it is
construed as too difficult to disentangle the impacts of feeding
from the multitudes of additional variables that influence bird
populations (1). We have demonstrated, however, that even with
a modest-scale experimental approach the impacts of feeding
can be readily observable. We stress that it is crucial to continue
assessing bird feeding in situ, where all other factors determining
avian community structure and ecology in urban areas still
operate, to gather realistic information on its effects. Outcomes
of feeding will vary with region as bird assemblages differ. We
expect, though, that granivores and omnivores benefit from
feeding to a greater degree than those in other dietary guilds,
regardless of whether they are introduced or native species, be-
cause provisioning of grain-based foods is the prevailing practice.
Methods
Study Site. This study was carried out at 24 urban, residential properties in
northern Auckland, New Zealand (Fig. 1), between January 2012 and De-
cember 2013. The North Shore area of Auckland is largely suburban resi-
dential, with a population density of 1,600/km
2
in 2006 (New Zealand Census
data, www.stats.govt.nz). Properties were recruited by word-of-mouth and
through local community groups. All properties offered for the study (n =
42) were visited before recruitment to assess suitability. Although the study
aimed to recruit householders whose properties were representative of the
whole study area, additional criteria were imposed to remove any extremely
different properties: gardens were required to have a minimum lawn area of
36 m
2
, trees > 2 m high on at least one boundary, be sited at least one
property away from any main road (experiencing constant traffic), and not
newly developed (within the last 5 y). Final selection of properties was de-
termined by the reliability of volunteers to adhere to the study guidelines,
accessibility, and distance to the nearest study property. All study properties
were greater than 350 m apart, to prevent repeat counts of the same birds,
although most (21 of 24) were >500 m apart.
Study properties were divided into two experimental treatment groups:
feeding (n = 12) or nonfeeding (n = 12). Allocation of experimental treat-
ment was determined by a two-step process. Householder preference was
first determined and strong preferences for treatment type were taken into
account, as to disregard these would risk the failure of participants to
comply with study guidelines. For the remaining properties (n = 16), the
treatment was randomly assigned using R 3.0.2 (R Development Core Team
2013). We had expected that retaining all households over the course of the
project would be difficult. However, only one feeding household withdrew
(after 12 wk) and was excluded from the analysis, leaving 11 feeding and 12
nonfeeding properties for the dura tion of the study.
Galbraith et al. PNAS
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Published online May 4, 2015
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E2655
ECOLOGY PNAS PLUS
Experimental Feeding Regime. Information obtained during the New Zealand
Bird Feeding Survey 2011 (11) provided the basis for the experimental
feeding regime. These results indicated that people feedi ng birds tended to
put out more than one type of food for birds (mean 2.42 types ± 0.06 SE, n =
505), so we opted for two food types for the feeding regime. Bread, the
most common food type fed to wild birds by the public (used by 88.1% of
feeding participants), was chosen as the first food type. Although fruit and
seed were fed by similar proporti ons of respondents (40.8% and 39.4%,
respectively) we selected seed as the second food type as it was logistically
easier to distribute to householders and to standardize quantities fed. Food
quantity was also determined using Galbraith et al. (11) and through a pilot
study used to assess the amount consumed in a single day. The aim was to
provide an abundant and reliable source of food for birds that was within
the range of that fed by the public. Hence, the experimental feeding treat-
ment consisted of: four to five slices of bread (several compositions but ex-
cluding white bread) and 1 metric cup of seed (budgie seed mix: white millet,
Hungarian millet, hulled oats, canary seed) provided on a daily basis for 18 mo.
Householders were asked to put out the food between 0700 and 0800 hours.
We ensured that all existing feeding practices at the study properties had
ceased 8 wk before the start of preliminary bird counts. A feeding station was
set up in each feeding garden, consisting of a low feeding table (17-cm high),
with a seed feeder and mesh bread tube fixed to it. Although a high pro-
portion of bird feeding participants in New Zealand simply throw food out
onto the groun d (11), the design of our feeding stations reflected the need
to have a structure capable of supporting a RFID antenna (for a separate
part of the project) and containers to prevent food being moved. House-
holders were given guidelines to follow, including cleanin g protocols, and
were responsible for provisioning the feeding stations. Householders in the
nonfeeding group were asked to refrain from putting supplementary food
of any kind out for birds for the duration of the study. At the end of the
feeding period, food provision was stopped immediately (i.e., no gradual
decrease). This regime was approved by the University of Auckland Animal
Ethics Committee (permit R921).
Avian Surveying. The method of surveying used in this study was dictated
by the nature of urban habitats. Counting birds in residential areas has a
number of challenges, in particular physical barriers (e.g., fences, buildings),
which prevent free movement of researchers through the landscape and
reduce the probability of detecting birds (54). Because of this we used point
counts from a fixed location, with a 10-min duration intended to increase
detectability of birds that were blocked from sight (55, 56). A point was
chosen on the study property that afforded the widest view of the sur-
rounding area. From this point, all birds seen or heard within the surrounding
radius over the 10-min survey duration were recorded. The survey radius
(approximately 80 m) was restricted by the physical and auditory barriers
associated with an urban setting. During the count, it was noted whether
individuals were using the habitat or were in transit (i.e., flying over the
survey area without stopping) with those in transit excluded from analyses.
A single experienced observer (J.A.G.) performed all counts.
Four preliminary counts were conducted at each study property from Jan-
uary to March at 2-wk intervals, after historical feeding practices had ceased
and before the start of experimental feeding. Counts were then conducted on a
monthly basis for the duration of the study, and continued for 4 mo after
feeding had ended [total counts, n = 597; note one count at a feeding property
was abandoned because of construction noise]. Counts were conducted in the
morning only, ∼1–5 h after sunrise. To visit all properties within this time-
frame, counts were conducted over 2 consecutive days. Study properties were
divided into four geographic blocks, with two of these blocks surveyed per
morning. Block order and property order within each block were randomly
assigned for each sampling round. Surveys were conducted in fine to fair
weather only; particularly wet or windy days were avoided.
Statistical Analyses. All statistical analyses were performed using R 3.0.2. The
critical α level was 0.05 for all tests. For species richness and overall abun-
dance analyses we removed incongruous species (those unlikely to use gar-
den habitat, e.g., shorebirds and wetland birds), most of which were present
in fewer than five counts. A list of all recorded species is given in Table S1,
with those retained for analyses indicated.
To analyze changes in avian community composition, we used three
nonparametric multivariate techniques: NMDS (57), PERMANOVA (58), and
PERMDISP (59). Data were split into experimental periods (before, during, and
after the feeding regime), and analyzed separately to: (i) check for differences
in avian community composition between feeding and nonfeeding properties
before the commencement of experimental feeding; (ii) determine whether
the experimental feeding regime had an effect on community composition;
and (iii) determine whether any observable changes persisted after feeding
had stopped. We used the Bray–Curtis measure of dissimilarity (60) as the
distance measure for all analyses, with species present in <5% of counts re-
moved (61); see Table S1 for included species. No transformation was applied
to the data before calculation of the distance-matrix, as we were specifically
interested in changes involving dominant species within bird communities.
To visualize differences in bird assemblages between feeding treatments, we
performed NMDS ordinations, using the metaMDS function of vegan v2.0-10
package (62) in R 3.0.2. Two-dimensional solutions were chosen and final ordi-
nations were generated from 250 random starts. Species centroids were plotted
separately to aid understanding of differences in avian community structure.
We used PERMANOVA analyses to test whether community compo-
sition varied between experimental groups in each experimental period.
PERMANOVA tests for differences in the locations (centroids) of multivariate
groups (63). Analyses were performed using the adonis function of vegan. P
values for the test statistic (pseudo-F) are based on 999 permutations, and
thus are reported down to, but not below, 0.001. We accounted for repeated
measures by including property ID as a random factor and by constraining
permutations to within properties (using the “strata” argument). We included
survey month number (categorical factor) as a fixed effect in the models, and
vegetation cover in the surrounding area (shrub/tree cover = 0–25% 26–50%,
51–75%) and background feeding level in the surrounding area (low, medium,
high) as random effects. “Surrounding area” refers to properties within a 100-m
radius of the focal property. Background feeding was determined in a concur-
rent study of local feeding practices (64). For the purposes of this modeling, we
scored background feeding as low where 0–33% of surrounding households
engaged in bird feeding, medium for 34–66%, and high for ≥67%. Vegetation
cover was estimated using aerial photography accessed April 4, 2014 from
Google Earth v7.1.2.2041 (Google Inc. 2013).
We tested for differences in the variability of bird assemblages between
feeding and nonfeeding properties with PERMDISP analyses for each experi-
mental period. Multivariate dispersions (distances of observations to their
centroids) were first calculated using the betadisper function of vegan, with the
mean dispersion then compared between groups via the permutest function
(constraining permutations within sites; based on 999 permutations). Where
designs are balanced, location vs. dispersion effects can be identified using
PERMANOVA and PERMDISP, respectively, with PERMANOVA tests remaining
reliable when heterogeneity in group dispersions is present (63).
Following the analysis of the community as a whole, we investigated the
effects of the feeding regime on species richness (overall, native, and in-
troduced), overall abundance, and the abundance of individual species. To do
this we used a GLMM approach (65), which was appropriate given the re-
peated-measures structure in the data. The distribution of each count vari-
able (species richness and abundances) was assessed and the best-fitting
distribution chosen for use in the corresponding models. The negative bi-
nomial distribution was found to be the best fit in most cases (see Table S2
for exceptions). Mixed-effect models were performed in R 3.0.2 using the
glmmPQL function in the MASS package (66). This function uses penalized
quasi-likelihood to estimate the model. The glmmPQL functio n requires the
dispersion parameter for the negative binomial model to be specified. This
was estimated for each model by running the equivalent nonmixed-effects
model with the glm.nb function, also from the MASS package.
For all models the experimental group (feeding or nonfeeding), experi-
mental period (before, during, or after), and the experimental group × ex-
perimental period interaction were included as fixed effects. The interaction
term tests the key study question of whether the feeding regime had an effect
on a given response variable, by comparing patterns of change from one ex-
perimental period to another between the two experimental groups. Property
ID was included as a random effect, to account for correlation of repeated
measures at the same properties. The time variable was used in the error
structure of the models. An autoregressive correlation structure of o rder 1
[AR(1)] was specified within each site, accounting for the fact that there may be
correlation among counts at the same property because of close proximity in
time. The corCAR1 function was used to specify this correlation with a con-
tinuous time covariate (days elapsed since the first count).
In addition, three factors with the potential to affect bird abundance were
also included in the models as control variables: the level of background feeding
in the surrounding area, the level of vegetation cover in the surrounding area,
and season (autumn, spring, summer, winter). The model predicted (or model
fitted) mean counts were calculated for each model, adjusting for these control
variables. The modeled means presented are averaged across the control
variables at the levels seen in the data (i.e., background feeding: 30% high, 61%
medium, 9% low; vegetation cover: 26% 0–25%, 48% 26–50%, 26% 51–75%),
except for season where each was represented equally (25%).
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www.pnas.org/cgi/doi/10.1073/pnas.1501489112 Galbraith et al.
ACKNOWLEDGMENTS. We thank the wonderful volunteer householders
involved in the study; EcoStock for donating food for the study; George
Perry for statistical advice and comments on the manuscript; Jessica McLay
for assistance with statistical analyses; and the Galbraith Family, Ellery
McNaughton, Cheryl Krull, Jo Peace, Megan Young, Sarah Wyse, Auckland
Zoo staff, and all who provided assistance in the field. This work was
supported in part by the Univer sity of Auckland, Auckland Council, and
Centre for Biodiversity and Biosecurity.
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