Urban Ecosyst
DOI 10.1007/s11252-017-0681-2

Urban environments are associated with earlier clutches
and faster nestling feather growth compared to natural habitats
Kristen L. D. Marini 1 & Ken A. Otter 2 & Stefanie E. LaZerte 2,3 & Matthew W. Reudink 1

# Springer Science+Business Media New York 2017

Abstract Urbanization creates new habitats with novel benefits and challenges not found in natural systems. How a species fares in urban habitats is largely dependent on its life
history, yet predicting the response of individual species to
urbanization remains a challenge. While some species thrive
in urban areas, others do poorly or are not present at all.
Mountain chickadees (Poecile gambeli) are year-round residents of montane regions of western North America.
Commonly found in higher-elevation coniferous forests, these
birds can also be found in urban areas where they will regularly visit bird feeders and nest in nest boxes. We monitored
mountain chickadees nesting along a habitat gradient, from
natural habitat to suburban areas, to determine if the degree
of urbanization was associated with: clutch size and success;
nestling growth rates; or variation in parental size and age.
Females nesting in urbanized areas initiated clutches earlier
in the breeding season than those in natural areas, but neither
fledging success nor the rate of nestling mass-change differed
between habitats. Nestling feather growth-rate increased with
later first egg dates in both habitats, and the magnitude of this
increase was greatest in urban habitats. We found no difference in the proportion of first-time breeders versus experienced breeders between habitat types, nor any differences in
male or female mass or size. Our results indicate no detriment

* Kristen L. D. Marini
kld.marini@gmail.com

1

Department of Biological Sciences, Thompson Rivers University,
900 McGill Road, Kamloops, BC V2C 0C8, Canada

2

Natural Resources and Environmental Studies, University of
Northern British Columbia, Prince George, BC, Canada

3

Department of Geography and Environmental Studies, Thompson
Rivers University, Kamloops, BC, Canada

to nesting in urban habitats, suggesting mountain chickadees
are able to adapt to moderate urbanization much like other
members of the Paridae family.
Keywords Reproductive success . Urbanization . Nestling
growth rate . Parental age . Parental size . Mountain
chickadee . Poecile gambeli
Urban habitats present new and unique challenges to birds and
are often associated with decreased species richness and diversity (Beissinger and Osborne 1982; Seress and Liker 2015),
but greater population densities of those species that thrive in
urban habitats (Marzluff 2001; Shochat 2004). Habitat modification and fragmentation associated with urbanization can
dramatically alter the structure and functionality of a habitat,
creating areas with novel combinations of challenges and benefits (Seress and Liker 2015). How a species fares in an urbanized area is highly dependent on its life history and ecology;
and species are often classified as: Burban exploiters^, those
species that can exploit the benefits of urbanization; Burban
avoiders^, those species that are highly sensitive to the disturbances of urbanization; or Burban adapters^, those species that
should be able to adapt to moderate levels of urbanization
(Blair 1996; Seress and Liker 2015).
For Burban exploiter^ species (e.g., European starling,
Sturnus vulgaris, and house sparrow, Passer domesticus,
Beissinger and Osborne 1982, Seress and Liker 2015;
American robin, Turdus migratorius, Morneau et al. 1995;
northern mockingbird, Mimus polyglottos, Stracey and
Robinson 2012), the shift into urban habitats allows for high
density and self-sustaining populations, which may be independent from rural populations. Urban habitats can provide benefits such as increased availability at nest sites (Sumasgutner
et al. 2014) and food resources, the latter of which may be from

Urban Ecosyst

novel sources, such as exotic plant species or birdfeeders (Robb
et al. 2008), improved foraging conditions (Stracey and
Robinson 2012), or from new prey species (Rutz 2008).
Urban habitats often have both a high abundance of food resources available (Anderies et al. 2007) and high stability of
these resources (Shochat 2004), potentially facilitating the
higher urban population densities for urban-exploiter and some
urban-adapter species (Marzluff 2001; Anderies et al. 2007).
Although there are potential benefits that allow some species
to thrive in urban environments, there are also challenges associated with urbanization, including habitat fragmentation
(Weldon and Haddad 2005), predation (Borgmann and
Rodewald 2004; Baker et al. 2008; Rodewald et al. 2010),
urban noise (Slabbekoorn and Ripmeester 2008; Slabbekoorn
2013), and increased chemical contaminants and pollution
(Burger et al. 2004). For urban-avoider species that are sensitive
to these disturbances, these urban challenges can lead to decreased survival and reproductive success (e.g., blue-grey gnatcatcher, Polioptila caerula, western wood-pewee, Contopus
sordidulus, Blair 1996; Acadian flycatcher, Empidonax
virescens, Rowse et al. 2014), and, in extreme cases, to significant population declines or even extirpation. For example, the
extirpation of the yellow-billed cuckoo, Coccyzus americanus,
from British Columbia, Canada is attributed to urban and agricultural development (Pearson and Healey 2012).
Urbanization causes habitat fragmentation, resulting in an
increased amount of edge habitat. While this can be preferred
by some urban-adapter species, nesting in areas with high
amounts of edgehabitats is associated with lowered reproductive success in others (e.g., indigo bunting, Passerina cyanea,
Weldon and Haddad 2005). Further, lower nest productivity,
smaller clutch sizes, and lower nestling mass in urban areas
are trends commonly seen across species (reviewed in
Chamberlain et al. 2009). Urban habitats may also be associated with increased nest predation rates for some species and
nest types (Gering and Blair 1999; Vincze et al. 2017); for
example, domestic cats (Felis catus) are abundant in many
urban areas and conservative estimates suggest they are responsible for 105 to 340 million bird deaths per year in
Canada (Blancher 2013; Loyd et al. 2013) and well over a
billion per year in the United States (Loss et al. 2013).
North American chickadees (genus Poecile) are good candidates to study the effects of habitat urbanization on avian
reproduction; there is an ample knowledge base on their behaviour and ecology (see Otter 2007), and they are commonly
found across most of Canada and the United States in both
their native rural forested areas and urban and suburban
habitats. Blewett and Marzluff (2005) determined that blackcapped chickadees (Poecile atricapillus) are found in lower
densities in urban areas, but have comparable reproductive
success to those in rural habitats. Yet, despite being a good
candidate group, little research has focussed on the impacts of
urbanization on chickadee reproduction.

There is significantly more information, however, on how
urbanization affects great tits (Parus major) and blue tits
(Cyanistes caeruleus), closely related European relatives of
chickadees. Wawrzyniak et al. (2015) found that great tits in
urban areas initiate clutches earlier but lay fewer eggs in urban
than in rural habitats, which also mirrors patterns found in
blue tits (Gladąlski et al. 2015). Likewise, Preiszner et al.
(2016) found that great tits breeding in urban areas had smaller
clutches, fewer fledglings, and lower mean fledgling mass
compared to those breeding in forested areas. These results
suggest, in some circumstances at least, that although tits
and flycatchers can breed in urban areas, they may be at a
disadvantage. In a recent cross-fostering study, Salmón et al.
(2016) found that nestling great tits reared in urban habitats
had significantly shorter telomere lengths than those reared in
rural areas, regardless of the habitat they were originally from,
suggesting that the stresses of urbanization may shorten
lifespan. However, a study examining the reproductive success of great tits, blue tits, and pied flycatchers (Ficedula
hypoleuca) nesting in man-made, suburban forest edges (golf
courses) found that not only did these species nest more readily in nest boxes on the edges of the golf courses than in the
surrounding forest, but these suburban nests also produced
more offspring (Saarikivi and Herczeg 2014).
Here, we aim to examine how urbanization influences the
reproductive dynamics of mountain chickadees (Poecile
gambeli). Specifically, we examine how nesting success, nestling growth rate, and adult mass, size, and breeding experience
differ between birds using nest boxes along an urbanization
gradient, from natural habitats to suburban and urban areas.
Mountain chickadees readily utilize artificial nest boxes, which
may provide an attractant to birds settling in urbanized landscapes. Unlike the relatively well-studied black-capped chickadee, mountain chickadees naturally inhabit coniferous forests;
thus urban environments in interior British Columbia, which
have abundant deciduous trees, represent strikingly different
habitat than their native woodlands. As such, we predicted that
mountain chickadees nesting in areas with increased urban features would 1) initiate nesting earlier in the season compared
their rural counterparts, but 2) have nestlings with reduced
growth rates, and 3) be primarily young, inexperienced breeders.

Methods
Study site
We collected data for this study in a 24 km2 study area around
Kamloops, British Columbia, Canada during the 2014 and
2015 breeding seasons. Our most natural, rural, study site
was located in Kenna Cartwright park (50°40.232′ N,
120°23.855′ W), an 800 ha wilderness park consisting of mature ponderosa pine (Pinus ponderosa) and Douglas fir

Urban Ecosyst

(Pseudotsuga menziesii) forests interspersed with grassland
and sagebrush (Artemisia tridentate) ground cover. The vegetation in this park is representative of the natural vegetation
of the region, with only minor disturbances in the form of
walking trails and a single low-traffic access road used for
park maintenance. We distributed 66 nest boxes throughout
the park, mounted approximately 2 m off the ground on mature trees, with 150 m between boxes. We distributed an additional 78 nest boxes across the Thompson Rivers University
campus and several neighbourhoods throughout the
Kamloops area to serve as urban/suburban study sites (see
Fig. 1 for all nest box locations). Urban neighbourhoods

Fig. 1 Nest boxes (yellow) were
distributed throughout
approximately a 24 km2 area
around the Kamloops, British
Columbia. Our natural study site
was located in Kenna Cartwright
Park (A), while our urbanized
study locations were located on
the Thompson Rivers University
campus (B), as well as through
several neighbourhoods through
southern Kamloops (C)

around Kamloops generally consist of a mixture of pine
Douglas fir with various species of native and non-native deciduous trees and shrubs. All boxes were cleaned and filled
with pine shavings after each breeding season.
Study species
Mountain chickadees are common resident songbirds found in
montane areas ranging from Baja California and Arizona
north to southern Yukon (McCallum et al. 1999). These secondary cavity nesters are typically found in mature conifer
forests, but will readily nest in artificial nest boxes when

Urban Ecosyst

available. Usually single brooded (McCallum et al. 1999),
average clutch size ranges from 5 to 8 eggs, and varies with
parental condition and environment (Dahlsten and Cooper
1979). Females incubate the eggs for an average of 14 days,
and nestlings typically fledge at 15–18 days old (Dahlsten and
Cooper 1979; McCallum et al. 1999). During the breeding
season, mountain chickadees eat and feed their nestlings various species of arthropods, while during the winter they rely
on stores of cached seeds or, in urban environments, seeds
from bird feeders (McCallum et al. 1999).
Data collection
Beginning in early May, we checked all boxes every four days
until we noted signs of nesting activity (e.g., excavated pine
shavings, signs of nest lining), after which all active nest boxes were checked every one to three days and inactive boxes
were checked once a week. Once the first egg was present we
checked nests every other day until clutches were complete.
We calculated expected hatch date based on a 14-day incubation period after the second to last egg was laid, and we
checked the nest daily from one day before the expected hatch
date until the eggs hatched, to determine hatching success.
Nestlings were banded with a uniquely-numbered
Canadian Wildlife Service (CWS) issued aluminum band at
6 days post hatch. When nestlings were 6 and 12 days old, we
weighed them to 0.1 g using a digital balance (AWS-250
Digital Scale), and recorded the length of the first primary
feather (P1) to 0.1 mm using callipers. These measurements
were consistently recorded in the morning, between 7:00 am
and 11:00 am. Changes in mass and feather length were then
used as indicators of nestling development rate (Ricklefs
1968; O’Connor 1978) and nutritional condition (Nowicki
et al. 2002). To avoid the risk of premature fledging, we did
not disturb the nestlings after day 12 until after their expected
fledging date on day 15. At this final check we recorded
fledging success based on the presence of any deceased nestlings remaining in the nest. Over two field seasons we monitored a total of 189 nestlings from 35 successful broods and 4
unsuccessful broods, with 88 nestlings from 16 nests in 2014
and 101 nestlings from 19 nests in 2015.
Between May 1st and June 26th, we captured adult chickadees on their territory either by simulating a territory intrusion by another male and catching them in a mist net, or by
trapping the parent in the nest box while they provisioned their
offspring. When parents had been captured on nests, we
returned to the nest at least an hour later and observed parents
with binoculars to ensure that they resumed regular behaviour
(i.e., provisioning, incubating); we observed no nest abandonment at these nests. Upon capture, we banded each individual
with a numbered CWS-issued aluminum band and a unique
combination of three coloured leg bands for individual identification. We determined age and sex according to Pyle

(1997), and recorded body mass, tail length, wing length (P1
feather), and tarsus lengths. Over the course of two field seasons we captured and collected data on a total of 26 female
and 25 male adult chickadees at their nests, with 16 females
and 11 males in 2014, and 10 females and 14 males in 2015
(some individuals were captured in both years).
Reproductive success and nestling growth rates
We obtained two measures of nestling growth rate, one from
nestling mass change and one from nestling feather growth.
Each was calculated as the residuals of a model regressing day
12 post-hatch measurements on day 6 post-hatch measurements (Lodjak et al. 2014). Positive residual values indicate
that growth rates were higher than the mean change based on
day 6 measurements (mass or P1 feather length), while negative residuals indicate that growth rates were lower than the
mean change. We calculated body mass and P1 length using
data from all nestlings that survived until day 12. Nestlings
that died before day 12 (n = 2) were excluded from calculations of growth rates (in both instances these nestlings died
before day 6), as were any nestlings missing either day 6 or
day 12 measurements. Nests that experienced full mortality
(n = 4) were not included in any analyses of growth or feather
growth rates.
In addition to nestling growth rates, we also determined
several measures of reproductive success. We recorded the
first egg date for each nest (in Julian dates), clutch size (total
number of eggs), the number of nestlings, hatching success
(eggs hatched/total eggs laid), number of fledglings, and
fledging success ([total nestlings – number of corpses remaining on day 18]/ total nestlings).
Habitat index
Some studies that examine the effects of urbanization compare
and contrast discreet urban versus rural categories (e.g.,
Beissinger and Osborne 1982), but classifying habitats, especially in suburban or interface habitat, is not always straightforward. To reduce subjectivity when dealing with these types
of habitats, a more objective approach can be to calculate an
index based on the ground cover type (e.g., natural vegetation
or man-made structures) and use that index to classify habitats
(Rolando et al. 1997; Dowling et al. 2012; LaZerte et al.
2017). Because our study sites varied along a gradient from
natural habitats to suburban neighbourhoods, a habitat index
was the most effective way to measure the variation in habitat
urbanization.
Following LaZerte et al. (2017), we used a combination of
manual and automated methods to create a habitat index for
the areas around our nest locations. First we extracted a map of
each nest box location from Google Earth (Google Inc 2012).
We then used an R script to plot a 75 m radius circle around

Urban Ecosyst

the nest box (roughly the size of an average territory), then
imported these into the image manipulation software GIMP
(The GIMP Team 2014), where we manually classified the
buildings, pavement, deciduous, and coniferous trees around
each nest location. Finally, we grouped buildings and pavement together as a single urban features variable, and used a
principal components analysis (PCA) in R v3.2.2 (R Core
Team 2017) to collapse deciduous trees, coniferous trees,
and urban features into a habitat urbanization index.
For our PCA, we retained the first principal component,
PC1, which accounted for 76% of the total variation in habitat
ground cover type. Larger PC1 values corresponded to increasing cover of coniferous trees (natural vegetation), with
decreasing amounts of urban features and deciduous trees
(non-native vegetation; PC1 loadings: coniferous trees = 0.532,
deciduous trees = −0.600, urban features = −0.596). Thus,
higher habitat index (PC1) values correspond to more coniferous forests representative of the natural habitat of the area,
with decreasing numbers of urban features and deciduous
trees (Fig. 2). This continuous measure of habitat index was
used in all statistical analyses.

Statistical analysis
We first constructed a generalized linear mixed model
(GLMM) with Poisson distribution and log link function with
first egg date as the response variable (n = 29 nests), and
habitat index, year, and their interaction as fixed effects.

Fig. 2 The distribution of habitat index scores was bimodal, with
negative scores indicative of habitats with increased urban features
(pavement and buildings) and deciduous trees (non-native vegetation),
and increasingly positive scores associated with decreased urban
features and deciduous trees and increases in coniferous trees (native
vegetation for the area)

Female band number nested within nest ID (each clutch was
assigned a unique nest ID) was included as a random effect.
We then constructed three GLMMs with Poisson distribution and log link function for measures of nesting
success (response variables: clutch size [n = 29 nests],
number of nestlings [n = 31 nests], and number of
fledglings [n = 31 nests]). Habitat index, year, first
egg date, and all two-way interactions were included
as fixed effects. Female band number nested within nest
ID was included as a random effect to control for the
influence of nestling being raised in a common environment. We excluded two nests from the analysis of first egg
date and clutch size; both were instances where the pair began
a second nest attempt on top of their first failed clutch, and
where we were unable to record an accurate first egg date for
the second nest attempt.
To examine how nestling growth rates varied with habitat
index, we also constructed a series of LMERs using measures
of nestling growth rate (nestling mass change, nestling feather
growth, day 12 nestling mass, and day 12 nestling P1 feather
length [n = 146 nestlings]) as the response variables. Habitat
index, year, first egg date, and all two-way interactions were
included as fixed effects. Female band number nested within
nest ID as a random effect. To ensure that nestling mass
change wasn’t unduly influenced by the number of nestlings
or paternal mass, we also ran our final nestling mass change
models including number of nestlings, as well as maternal and
paternal mass as covariates.
Because adult size and condition can influence offspring
provisioning rates, and thus offspring survival (Tveraa et al.
1998; Nager et al. 2000), we used linear models to investigate
whether adult body size (mass, P1 wing length, tail length,
tarsus length) varied with habitat index, year, capture date,
and all two-way interactions. We constructed separate models
for males (n = 19) and females (n = 23) resulting in 10 models
(5 models for each sex).
Finally, we constructed two GLMMs with binomial
distribution and logit link function to examine if there were
differences in the proportion of first-year breeders (individuals
aged as second year, SY) or older breeders (individuals aged
as after second year, ASY) between habitats. Parental age was
the response variable and we included habitat index, year and
their interaction as fixed effects. Individual band number was
included as a random effect. We constructed separate models
for males (n = 23) and females (n = 26).
In all models, we used a stepwise removal of nonsignificant (p > 0.05) variables to determine the final
best fit model. All statistical analyses were conducted
in R version 3.3.3 (R Core Team 2017). Linear mixed models
were created using the Blme4^ (version 1.1–12, Bates et al.
2015) and BlmerTest^ (version 2.0–33, Kuznetsova et al.
2016) packages for R, and figures were made using JMP 12
(SAS Institute 2015).

Urban Ecosyst

Ethical note
This research was carried out under Thompson Rivers
University Animal Care and Use Protocol no. 100846,
University of Northern British Columbia Animal Care and
Use Protocol no. 2014–06, and under Canadian Wildlife
Service collection permit no. 22806.

Results
Nesting success
Mountain chickadees nesting in habitats with more urban features (lower habitat index) initiated clutches earlier than those
in natural habitats (higher habitat index; Table 1; Fig. 3); mean
first egg date (± SD) was April 26 ± 5.6 days for pairs in urban
habitat and May 15 ± 7 days for pairs in natural habitat. Clutch
size did not differ with habitat index, year or first egg date, nor
did the number of nestlings, or the number of fledglings
(Table 2).
Nestling growth rates
Both first egg date and habitat index were strong predictors of
feather growth rate, and there was a significant interaction
between first egg date and habitat index (Table 3). Feather
growth rate increased with later first egg dates, but this increase was more rapid in habitats with more urban features
and deciduous trees (lower habitat index; Fig. 4). We found no
association between the rate of nestling mass change and habitat index, year or first egg date (Table 3), even when we
included covariates such as the number of nestlings (all
p > 0.10), maternal mass (all p > 0.11), or paternal mass (all
p > 0.39). On day 12, at our last measurements prior to the
expected fledging on day 15, we found no effects of habitat
index on either nestling mass or P1 feather length (Table 4).
Adult age and size by habitat
We found no relationship between female age, wing length,
tail, or tarsus, and habitat index (Table 4). The relationship
between habitat index and female mass approached significance (p < 0.08), showing a slight trend for urban females to

Fig. 3 Chickadee pairs nesting in habitats with more urban features and
more deciduous trees (negative values) began nesting earlier than those
pairs nesting in more natural habitats (positive values)

have a greater mass. Likewise, we found no relationship between male mass, or body measurements, and habitat index
(Table 5). However, we did find that capture date was a significant predictor of both wing and tarsus length in male
chickadees, where P1 wing length and tarsus each decreased
with later capture dates (Table 5). There were no relationships
between age and habitat index for either male or female mountain chickadees (Table 6).

Discussion
The timing of mountain chickadee reproduction and the rate
of nestling feather growth varied along a habitat gradient from
natural to urbanized habitats. Our finding that pairs in urbanized habitats initiate clutches earlier is consistent with findings
in other species, including blue tits and great tits (reviewed in
Chamberlain et al. 2009; Gladąlski et al. 2015; Wawrzyniak
et al. 2015); however, unlike in previous research on other
species (reviewed in Lack 1947; Perrins and McCleery
Table 2 Final best fit GLMMs examining the effects of habitat index,
year, and first egg date on clutch size, number of nestlings, or number of
fledglings in mountain chickadees. Significant results are bolded
Factor

Table 1 Final best fit GLMMs examining the effects of habitat index
and year on the first egg date in mountain chickadees. Significant results
are bolded
1st Egg date
Factor
Habitat Index

Estimate
0.04

SE
0.012

z
3.33

n
29

p
0.0009

Estimate

Clutch size
1st Egg date
−0.005
Number of nestlings
1st Egg date
−0.01
Number of fledglings
1st Egg date
−0.01

SE

z

n

p

0.007

−0.76

29

0.45

0.007

−1.49

31

0.14

.000

−1.59

31

0.11

Urban Ecosyst
Table 3 Final best fit LMERs examining the effects of habitat index,
year, and first egg date on nesting mass change and feather growth in
mountain chickadees. Significant results are bolded

Table 4 Final best fit LMERs examining the effects of habitat index,
year, and first egg date on day 12 mass and P1 feather length in nestling
mountain chickadees

Factor

Factor

Estimate SE

t

n

p

Feather growth
1st Egg date

SE

t

n

p

−0.07

0.07

−0.90

146

0.38

Standardized day 12 P1 by year
Habitat index
0.62
0.61

1.02

146

0.32

Day 12 mass
0.76

Urbanization index
−0.45
1st Egg date*urbanization index −0.41
Mass change
Habitat index

Estimate

−0.06

0.21 3.64

146 0.002

0.13 −3.52 146 0.002
0.14 −2.88 146 0.001

Habitat index

0.08 −0.78 146 0.44

1989; reviewed in Chamberlain et al. 2009), we found no
seasonal decline in clutch size. Although females in urbanized
areas began laying significantly earlier than those in natural
habitats, the average number of eggs and fledglings did not
differ between habitats. In many species, early breeding has
been linked to reproductive benefits such as higher reproductive success (Perrins 1970; Wilson and Arcese 2003; reviewed
in Verhulst and Nilsson 2008; Reudink et al. 2009; Germain
et al. 2015; but see Visser et al. 1998; Penteriani et al. 2014)
and an increased likelihood of attempting a second brood
(Townsend et al. 2013), however, we found no evidence of
reproductive advantaged in our study population.
We also found a relationship between nestling feather
growth rate and habitat, though the relationship contradicted
our predictions; specifically, feather growth rates were highest
in urban habitats and in later-initiated nests, and the increase in
growth rates as the season progressed was most rapid in urban

habitats (Fig. 4). This faster feather development could suggest that nestlings in urbanized areas were being better provisioned, allowing for faster growth rates (Searcy et al. 2004).
However, we only found an increase in nestling feather
growth rate and not also in the rate of mass gain. In light of
this, the increased feather growth rates could reflect urban
nestlings growing faster, but lower-quality feathers, and future
studies examining feather quality (e.g., feather mass, fault
bars) could help identify the cause of the increased feather
growth. Alternatively, there may be multiple factors influencing nestling growth which promote faster feather growth but
not mass gain.
It is likely that the habitat-related difference first egg date
we found in this study is caused, at least in part, by differences
in winter food availability. Urban habitats generally have high
food resource abundance and stability (Anderies et al. 2007),
and indeed, there was often at least one bird feeder in close
proximity to each of our urban nests (K. Marini, personal
observation). Bird feeders provide consistent availability of
Table 5 Final best fit linear models examining the effects of habitat
index, year, and capture date on mass, fat score, wing, tail, and tarsus
length of adult chickadees. Significant results bolded
Factor

Estimate

SE

t

n

p

−0.13

0.07

−1.87

23

0.08

−0.03

0.02

−1.20

22

0.24

0.14

0.82

0.17

22

0.87

−0.01

0.008

−1.58

22

0.13

−0.22

0.26

−0.83

19

0.42

−0.08

0.03

−2.68

19

0.02

−0.10

0.04

−2.62

19

0.02

0.05

0.06

0.94

19

0.36

Female mass

Fig. 4 Nestling feather growth rate increased with later first egg dates,
but was more rapid in urbanized habitats (dashed line, open circles) than
in natural ones (solid line, black dots). For ease of interpretation, we
presented the results with habitat index split into discreet categories,
where 0.70 and greater was classed as natural and −0.50 and below
classes as urbanized habitat

Habitat Index
Female wing
Capture date
Female tail
Year
Female tarsus
Capture date
Male mass
Year
Male wing
Capture date
Male Tail
Capture date
Male tarsus
Habitat index

Urban Ecosyst
Table 6 Final Best fit GLMMs examining the effects of habitat index
and year on age of female and male mountain chickadees
Factor

Estimate

SE

z

n

p

Habitat

0.28

0.36

0.79

21

0.43

Male age
Year

0.76

1.08

0.70

19

0.48

Female age

food resources through the winter, while birds in natural habitats have to rely on food caches (Sherry 1984), a limited and
potentially unreliable food source. The stability and abundance of winter food from urban bird feeders could allow
females to maintain a higher overwintering mass and physical
condition, and thus allow them to reach egg laying condition
earlier than those females living in natural habitats. An alternative explanation, or potentially a contributing explanation,
is that differences in the timing of peak insect abundance differ
with habitat (e.g., see great tits, Van Noordwijk et al. 1995),
which thus influences the timing of breeding.
Previous research has established that diet has a strong
influence on nestling growth rates, especially on characteristics such as mass (Boag 1987). Our finding that urban chickadees experienced a higher feather growth rates could be due
to greater access to food resources during the breeding season.
When we analyzed ground cover type around the nest boxes
while creating the habitat index, it revealed that of all the trees
present in a 75 m radius around each nest box, an average of
0.2% were deciduous in natural areas, while in urbanized
areas 31.2% were deciduous. In general, deciduous trees are
associated with a greater diversity and abundance in insect
species compared to conifers (Southwood 1961), but urban
environments also tend to have many non-native plant species
which may also impact insect prey item availability (Issacs
et al. 2009). If urban habitats have a greater availability of
food resources, parents in the food-limited rural habitats may
then have to increase their foraging effort to provide adequate
food to their offspring (Tremblay et al. 2005), constraining the
growth rates. Alternatively, the increase in feather growth rate
may mean that urban nestlings could be growing lowerquality feathers, as previous studies have found that feather
growth rate and feather quality are negatively correlated in
adults (de la Hera et al. 2009). Regardless, just prior to fledging (day 12), neither nestling mass nor P1 length differed
between habitats, suggesting that nestlings are likely not nutritionally advantaged or disadvantaged in either habitat.
There were no differences in adult size or mass between
habitats, nor any differences in the proportions of experienced
and inexperienced breeders, suggesting that urbanized habitat
is not being actively avoided by older, experienced birds and
is therefore likely perceived as being equivalent quality to
natural habitats. The finding that male P1 wing length

decreased with later capture dates potentially is due to feather
wear as the season progresses, especially since the difference
was only ~2–3 mm. The season decrease in tarsus length
measurements was likely due to observer error in the early
season, as all the measurements fell within a 1.4 mm range.
Indeed, our findings indicate no reproductive disadvantage to
nesting in urban environments for mountain chickadees.
Alternatively, the chickadees in our urban study sites could
be settled in the pockets of good habitat amongst habitat that is
generally of lower quality, or, our sample size may have been
too small to detect any differences in adult size, mass or age.
Because we relied heavily upon volunteers in the community
to put up nest boxes on their property, most of the nest boxes
were located in yards of naturalists with bird feeders up
through the winter. Though some (n = 4) of our urban nests
were in locations without consistent bird feeder access nearby
(as far as we could discern), most active urban nests were in
close proximity to bird feeders. Thus, our nest sites could have
been in areas where the winter habitat quality had been artificially increased (Robb et al. 2008), resulting in heavier, potentially better condition chickadees in the pre-breeding season relative to urban areas without winter feeder access.
Future studies examining nestling diet may help us determine differences in the abundance and diversity of insects in
urban and rural habitats (e.g., through the use of frass traps,
sweep nets, and observations of nestling provisioning) and
how these differences influence nestling mass change and
feather growth rate. Another area of future study would be to
compare the timing of peak insect abundance between habitats
and determine if this is related to the differences we found in
first egg date. These types of study would help determine if
urban habitats are, generally, of comparable quality to rural
habitats, as well as help in determine if differences in peak
insect abundance in the different habitats influences the differences we see in first egg dates.
An important limitation of our current study is that many of
our more Burban^ nests were in suburban areas, as most
mountain chickadees were found around suburban residential
areas rather than in the most highly urbanized habitats (e.g.,
see eBird mountain chickadee sightings for the Kamloops area
from 2014 to 2016; Sullivan et al. 2009), likely due to the lack
of suitable nest sites and foraging habitats, as well as the fact
that the most urbanized locations in Kamloops are located at
lower elevations where black-capped chickadees predominate. Another set of limitations are that our study does not
account for any potential differences in predation rates, mortality rates after fledging, or overall lifespan – all of which are
important, but notoriously difficult to obtain.
Overall, urban female mountain chickadees initiate
clutches earlier than those in natural areas, and both this difference in clutch initiation and the increase in feather growth
rate may suggest increased food availability. Our results support previous research which suggests, for some insectivorous

Urban Ecosyst

species, urban areas may provide a greater amount of food
resources (Anderies et al. 2007; reviewed in Chamberlain
et al. 2009; but see Marciniak et al. 2007). Unlike some bird
species (reviewed in Chamberlain et al. 2009), mountain
chickadees did not experience lower nestling mass or lower
productivity in urban areas. Similar to previous results seen in
great tits and blue tits (Gladąlski et al. 2015; Wawrzyniak et al.
2015; Preiszner et al. 2016; Bailly et al. 2016), the chickadees
in our study did not have increased clutch sizes or numbers of
offspring. A possible causal mechanism for the lack of a negative effect of urbanization may be the shift in predominant
tree species in urban areas; despite a lower overall canopy
cover and increasing urban features, the trees that were present
in our urban landscapes shifted from coniferous to deciduous
species. The higher insect abundance typically associated with
deciduous species compared to coniferous species may have
offset the lower total canopy from which to forage in urban
sites, making the two habitats more similar in overall quality.
This shift in habitat features may allow mountain chickadees
to be urban adaptors, like many other members of the Paridae
family (Croci et al. 2008).
Acknowledgements The authors would like to thank S. Joly and members of the BEAC Lab at Thompson Rivers University for assisting with
the capture and banding of chickadees, as well as all the field technicians
who assisted with data collection and field work. Funding was provided
by Natural Sciences and Engineering Research Council of Canada
Discovery Grants to M.W.R. and K.A.O, and a Natural Sciences and
Engineering Research Council of Canada Industrial Postgraduate
Scholarship to K.L.D. Marini.

References
Anderies J, Katti M, Shochat E (2007) Living in the city: resource availability, predation, and bird population dynamics in urban areas. J
Theor Biol 247:36–49
Bailly J, Scheifler R, Berthe S, Clément-Demange V, Leblond M, Pasteur
B, Faivre B (2016) From eggs to fledging: negative impact of urban
habitat on reproduction in two tit species. J Ornithol 157:377–392
Baker P, Molony S, Stone E, Cuthill I, Harris S (2008) Cats about town: is
predation by free-ranging pet cats Felis catus likely to affect urban
bird populations? Ibis 150:86–99
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixedeffects models using lme4. J Stat Softw 67:1–48
Beissinger S, Osborne D (1982) Effects of urbanization on avian community organization. Condor 84:75–83
Blair R (1996) Land use and avian species diversity along an urban
gradient. Ecol Appl 6:506–519
Blancher P (2013) Estimated number of birds killed by house cats (Felis
catus) in Canada. Avian Conserv Ecol 8:3
Blewett C, Marzluff J (2005) Effects of urban sprawl on snags and the
abundance and productivity of cavity-nesting birds. Condor 107:
678–693
Boag P (1987) Effects of nestling diet on growth and adult size of zebra
finches (Poephila guttata). Auk 104:155–166
Borgmann K, Rodewald A (2004) Nest predation in an urbanizing landscape: the role of exotic shrubs. Ecol Appl 14:1757–1765

Burger J, Bowman R, Wooldenden G, Gochfeld M (2004) Metal and
metalloid concentrations in the eggs of threatened Florida scrubjays in suburban habitats from south-central Florida. Sci Total
Environ 328:185–193
Chamberlain D, Cannon A, Toms M, Leech D, Hatchwell B, Gaston K
(2009) Avian productivity in urban landscapes: a review and metaanalysis. Ibis 151:1–18
Croci S, Butet A, Clergeau P (2008) Does urbanization filter birds on the
basis of their biological traits? Condor 110:223–240
Dahlsten DL, Cooper WA (1979) The use of nesting boxes to study the
biology of the mountain chickadee (Parus gambeli) and its impact
on selected forest insects. In: Dickson JG, Connor RN, Fleet RR,
Jackson JA, Kroll JC (eds) The role of insectivorous birds in forest
ecosystems. Academic Press, New York, pp 217–260
de la Hera I, Pérez-Tris J, Tellería J (2009) Migratory behaviour affects
the trade-off between feather growth rate and feather quality in a
passerine bird. Biol J Linn Soc 97:98–105
Dowling J, Luther D, Marra P (2012) Comparative effects of urban development and anthropogenic noise on bird songs. Behav Ecol 23:
201–209
Gering J, Blair R (1999) Predation on artificial bird nests along an urban
gradient: predatory risk or relaxation in urban environments?
Ecography 22:532–541
Germain R, Schuster R, Delmore K, Arcese P (2015) Habitat preference
facilitates successful early breeding in an open-cup nesting songbird.
Funct Ecol 29:1522–1532
Gladąlski M, Bańburna M, Kaliński A, Markowski M, Skwarska J,
Wawrzyniak J et al (2015) Inter-annual and inter-habitat variation
in breeding performance of blue tits (Cyanistes caeruleus) in central
Poland. Ornis Fennica 92:34–42
Google Inc (2012) Google Earth http://google.com/earth/
Issacs R, Tuell J, Fiedler A, Gardiner M, Landis D (2009) Maximizing
arthropod-mediated ecosystem services in agricultural landscapes:
the role of native plants. Front Ecol Environ 7:196–203
Kuznetsova A, Brockhoff P, Christensen R (2016) lmerTest: tests in linear
mixed effects models. R package version 2.0-33
Lack D (1947) The significance of clutch-size. Ibis 89:302–352
LaZerte S, Otter K, Slabbekoorn H (2017) Mountain chickadees adjust
songs, calls and chorus composition with increasing ambient
and experimental anthropogenic noise. Urban Ecosys. doi:
10.1007/s11252-017-0652-7
Lodjak J, Mägi M, Vallo T (2014) Insulin-like growth factor 1 and growth
rate in nestlings of a wild passerine bird. Funct Ecol 28:159–166
Loss S, Will T, Marra P (2013) The impact of free-ranging domestic cats on wildlife of the United States. Nat Commun 4:
1396. doi:10.1038/ncomms2380
Loyd K, Hernandez S, Carroll J, Abernathy K, Marshall G (2013)
Quantifying free-roaming domestic cat predation using animalborne video cameras. Biol Conserv 160:183–189
Marciniak B, Nadolski J, Nowakowska M, Loga B, Bańbura J (2007)
Habitat and annual variation in arthropod abundance affects blue tit
Cyanistes caeruleus reproduction. Acta Ornithologica 42:53–62
Marzluff J (2001) Worldwide urbanization and its effects on birds. In:
Marzluff J, Bowman R, Donnelly R (eds) Avian ecology and conservation in an urbanizing world. Kluwer Academic Publishers,
Springer, US, pp 19–38
McCallum DA, Grundel R, Dahlsten DL (1999) In: Poole A (ed)
Mountain chickadee (Poecile gambeli), the birds of North America
online. Cornell Lab of Ornithology, New York. doi:10.2173/bna.453
Morneau F, Lépine C, Décarie R, Villard M, Des Granges J (1995)
Reproduction of American robin (Turdus migratorius) in a suburban
environment. Landsc Urban Plan 32:55–62
Nager R, Monaghan P, Houston D, Genovart M (2000) Parental condition, brood sex ratio and differential young survival: an experimental
study in gulls (Larus fuscus). Behav Ecol Sociobiol 48:452–457

Urban Ecosyst
Nowicki S, Searcy W, Peters S (2002) Brain development, song learning
and mate choice in birds: a review and experimental test of the
Bnutritional stress hypothesis^. J Comp Physiol A 188:1003–1014
O’Connor R (1978) Structure in avian growth patterns: a multivariate
study of passerine development. J Zool (Lond) 185:147–172
Otter K (ed) (2007) Ecology and behavior of chickadees and titmice: an
integrated approach. Oxford University Press, New York
Pearson M, Healey M (2012) Species and risk and local government: a
primer for BC. Stewardship Center of British Columbia, Courtenay
(BC) http://www.speciesatrisk.bc.ca/node/8055
Penteriani V, Delgado M, Lokki H (2014) Global warming may depress
avian population fecundity by selecting against early-breeding,
high-quality individuals in northern populations of single-brooded,
long-lived species. Ann Zool Fenn 51:390–398
Perrins C (1970) The timing of birds’ breeding season. Ibis 112:242–255
Perrins C, McCleery R (1989) Laying dates and clutch size in the great tit.
Wilson Bull 101:236–253
Preiszner B, Papp S, Pipoly I, Seress G, Vincze E, Liker A,
Bókony V (2016) Problem-solving performance and reproductive success of great tits in urban and forest habitats.
Anim Cogn. doi:10.1007/s10071-016-1008-z
Pyle P (1997) Identification guide to North American birds. Part 1. Slate
Creek Press, Bolinas
R Core Team (2017) R: a language and environment for statistical computing. Version 3.3.3. R Foundation for Statistical Computing.
Vienna. https://www.R-project.org/. Accessed 3 March 2017
Reudink MW, Marra PP, Kyser TK, Boag PT, Langin KM, Ratcliffe LM
(2009) Non-breeding season events influence sexual selection in a
long-distance migratory bird. Proc R Soc B 276:1619–1626
Ricklefs R (1968) Patterns of growth in birds. Ibis 110:419–451
Robb G, McDonald R, Chamberlain D, Bearhop S (2008) Food for
thought: supplementary feeding as a driver of ecological change in
avian populations. Front Ecol Environ 6:476–484
Rodewald A, Shustack D, Hitchcock L (2010) Exotic shrubs as ephemeral ecological traps for nesting birds. Biol Invasions 12:33–39
Rolando A, Maffei G, Pulcher C, Giuso A (1997) Avian community
structure along an urbanization gradient. Ital J Zool 64:341–349
Rowse L, Rodewald A, Sullivan S (2014) Pathways and consequences of
contaminant flux to Acadian flycatchers (Empidonax virescens) in
urbanizing landscapes of Ohio, USA. Sci Total Environ 485-486:
461–467
Rutz C (2008) The establishment of an urban bird population. J Anim
Ecol 77:1008–1019
Saarikivi J, Herczeg G (2014) Do hole-nesting passerine birds fare well at
artificial suburban forest edges? Ann Zool Fenn 51:488–494
Salmón P, Nilsson J, Nord A, Bensch S, Isaksson C (2016) Urban environment shortens telomere length in nestling great tits, Parus major.
Biol Lett 12:20160155
SAS Institute (2015) JMP®, Version 12. SAS Institute Inc, Cary
Searcy W, Peters S, Nowicki S (2004) Effects of early nutrition on growth
rate and adult size in song sparrow Melospiza melodia. J Avian Biol
35:269–279
Seress G, Liker A (2015) Habitat urbanization and its effects on birds.
Acta Zool Acad Sci 61:373–408
Sherry D (1984) Food storage by black-capped chickadees: memory for
the location and contents of caches. Anim Behav 32:451–464

Shochat E (2004) Credit or debit? Resource input changes population
dynamics of city-slicker birds. Oikos 106:622–626
Slabbekoorn H (2013) Songs of the city: noise-dependent spectral plasticity in the acoustic phenotype of urban birds. Anim Behav 85:
1089–1099
Slabbekoorn H, Ripmeester E (2008) Birdsong and anthropogenic noise:
implications and applications for conservation. Mol Ecol 17:72–83
Southwood T (1961) The number of species of insect associated with
various trees. J Anim Ecol 30:1–8
Stracey C, Robinson S (2012) Are urban habitats ecological traps for a
native songbird? Seasonal productivity, apparent survival, and site
fidelity in urban and rural habitats. J Avian Biol 43:50–60
Sullivan B, Wood C, Iliff M, Bonney R, Fink D, Kelling S (2009) eBird: a
citizen-based bird observation network in the biological sciences.
Biol Conserv 142:2282–2292
Sumasgutner P, Nemeth E, Tebb G, Krenn H, Gamauf A (2014) Hard
times in the city – attractive nest sites but insufficient food supply
leads to low reproductive success rates in a bird of prey. Front Zool
11:48–61
The GIMP Team (1997-2014) GIMP 2.8.10. https://www.gimp.org
Townsend A, Sillett T, Lany N, Kaiser S, Rodenhouse N, Webster
M, Holmes R (2013) Warm springs, early lay dates, and
double brooding in a North American migratory songbird,
the black-throated blue warbler. PLoS One 8:e59467. doi:
10.1371/journal.pone.0059467
Tremblay I, Thomas D, Blondel J, Perret P, Lambrechts M (2005) The
effect of habitat quality on foraging patterns, provisioning
rate and nestling growth in Corsican blue tits Parus
caeruleus. Ibis 147:17–24
Tveraa T, Sether E, Aanes R, Erikstad K (1998) Regulation of food
provisioning in the Antarctic petrel; the importance of parental body
condition and chick body mass. J Anim Ecol 67:699–704
Van Noordwijk A, McCleery R, Perrins C (1995) Selection for the timing
of great tit breeding in relation to caterpillar growth and temperature.
J Anim Ecol 64:451–458
Verhulst S, Nilsson J (2008) The timing of birds’ breeding seasons: a
review of experiments that manipulated timing of breeding. Philos
Trans R Soc B 363:399–410
Vincze E, Seress G, Lagisz M, Nakagawa S, Dingemanse N, Sprau P
(2017) Does urbanization affect predation of bird nests? A metaanalysis. Front Ecol Evol 5:29
Visser M, van Noordwijk A, Tinbergen J, Lessells C (1998) Warmer
springs lead to mistimed reproduction in great tits (Parus major).
Proc R Soc Lond Biol 265:1867–1870. doi:10.1098/rspb.1998.0514
Wawrzyniak J, Kaliński A, Glądalski M, Bańbura M, Markowski
M, Skwarska J et al (2015) Long-term variation in laying
date and clutch size of the great tit Parus major in central
Poland: a comparison between urban parkland and deciduous
forest. Ardeola 62:311–322
Weldon A, Haddad N (2005) The effects of patch shape on indigo buntings: evidence for an ecological trap. Ecology 86:1422–1431
Wilson S, Arcese P (2003) El Niño drives timing of breeding but not
population growth in the song sparrow (Melospiza melodia). Proc
Natl Acad Sci U S A 100:1139–1142