Urban Ecosystems (2019) 22:1113–1122
https://doi.org/10.1007/s11252-019-00884-4

Caterpillar phenology predicts differences in timing of mountain
chickadee breeding in urban and rural habitats
Adrianne C. Hajdasz 1 & Ken A. Otter 2 & Lyn K. Baldwin 1 & Matthew W. Reudink 1
Published online: 29 July 2019
# Springer Science+Business Media, LLC, part of Springer Nature 2019

Abstract
To ensure the survival of their offspring, birds need to precisely time their reproduction: when offspring have the highest demand for
food, food resources should be most abundant. In temperate environments, caterpillars are often a key food source for nestlings, so
many insectivorous bird species time their reproduction to correspond to the peak abundance of caterpillars in their habitat.
Mountain chickadees (Poecile gambeli) are small songbirds that naturally inhabit coniferous forests, but are also found in urban
areas. Reproductive timing of these birds may be altered by urbanization, as mountain chickadees in the city have been shown to
breed earlier than those in natural habitat. This study aimed to determine if caterpillar abundance drives reproductive timing of
mountain chickadees and if urbanization alters the timing of caterpillar abundance. Birds in both urban and rural habitats were
monitored throughout the breeding season. Caterpillar abundance was estimated at each nest location by collecting samples of
caterpillar excrement (frass). We found that in both urban and rural habitat, frass mass changed throughout the breeding season, but
the date of maximum frass mass occurred about one week earlier in urban habitat. However, in both habitats maximum frass mass
occurred when offspring were approximately 11 days old. Our results suggest that mountain chickadees time their reproduction to
correspond to caterpillar abundance, and birds in urban environments may be reproducing earlier to correspond with earlier peak
caterpillar abundance in the city.
Keywords Frass . Urbanization . Reproductive timing . Caterpillar . Mountain chickadee . Poecile gambeli

Introduction
To maximize reproductive success, many seasonally breeding
birds precisely time their reproduction to correspond to maximum food availability for their offspring (reviewed in Davies
and Deviche 2014). However, this requires making decisions
about when to breed several weeks before those resources are
maximally available. To do so, birds may rely on cues such as
photoperiod (Dawson et al. 2001), temperature (Van
Noordwijk et al. 1995), and leaf phenology (Nilsson and
Källander 2006) to predict when food sources will be most
abundant. In most temperate regions, caterpillars are a key
* Matthew W. Reudink
mreudink@tru.ca
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

resource for many insectivorous birds. Caterpillars and spiders
are the two most common insects consumed by tits and chickadees (Nour et al. 1998; Smith 1992); however, evidence suggests caterpillars are a higher-quality food resource as blue tit
(Cyanistes caeruleus) populations that fed their young a higher
proportion of caterpillars than spiders had greater reproductive
success than blue tit populations that fed their young diets with
a higher proportion of spiders (Blondel et al. 1991). Caterpillars
may be an important food source in warm climates, as compared with spiders they contain a much higher water content,
essential for maintaining water balance in nestlings (reviewed
in Blondel et al. 1991). Caterpillars also contain high protein,
fat and micronutrient content, making them a valuable prey
group (Razeng and Watson 2015). In some regions, especially
Europe, caterpillars have a short peak in abundance of only a
few weeks after bud burst of deciduous trees (Van Balen 1973;
Perrins 1991). Therefore many woodland birds use predictive
cues to time their reproductive cycles so that caterpillar peak
abundance coincides with highest nestling demand for food
(Perrins 1970; Perrins 1991; Van Noordwijk et al. 1995;

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Hinks et al. 2015). Tits even appear to prefer certain families of
lepidoptera larvae, and show reduced reproductive success
when they are unable to time their reproduction to correspond
with maximum abundance of preferred species (García-Navas
and Sanz 2011).
Mistiming of breeding in relation to caterpillar abundance
can have serious fitness consequences. For example, great tits
(Parus major) that had their clutches experimentally removed
and were forced to initiate a second clutch late in the breeding
season had clutch size, nestling mass and fledging success
significantly reduced compared to controls (Verhulst and
Tinbergen 1991). Similarly, classic studies on Mediterranean
blue tits demonstrated the importance of habitat-specific reproductive timing. Birds that were unable to time reproduction
to correspond to peaks in food availability produced ~30%
fewer eggs (Blondel et al. 1993). Warming temperatures that
result from climate change can advance leaf phenology and
insect emergence, also resulting in mistiming of reproduction
(reviewed in Visser and Both 2005 and Cleland et al. 2007).
Some bird populations (e.g., great tits in England) have successfully adjusted their reproductive timing in response to
climate change; warmer spring temperatures have advanced
peak caterpillar abundance by about 2 weeks, with tits now
responding by laying eggs approximately 2 weeks earlier
(Charmantier et al. 2008). However, not all bird populations
are able to adapt to climate change; although warmer spring
temperatures in Holland have advanced peak caterpillar biomass, a Dutch population of great tits has not been able to
advance their laying enough to keep their reproductive timing
in sync (Visser et al. 1998, 2006). This mismatch of reproductive timing and resource availability has reduced fitness in this
population (Nussey et al. 2005). Dutch populations of pied
flycatchers (Ficedula hypoleuca) have similarly been unable
to advance their arrival date on the breeding ground to correspond with warming spring temperatures (Both and Visser
2001). This mismatch prevents birds from laying their eggs
early enough to synchronize with peak insect abundance and
as a result, reproductive success is reduced significantly; areas
with the earliest caterpillar peaks were associated with a 90%
decline in population size (Both et al. 2006).
Parallel to climate change, urbanization is associated with
increased temperatures—a phenomenon known as the urban
heat island effect (Imhoff et al. 2010). Other factors associated
with urbanization, such as increased rainfall, nonnative species, man-made structures, and alternative food sources
(reviewed in McKinney 2002), also have the potential to alter
prey abundance, plant and animal phenology, and the reproductive success of birds. For instance, urban areas are associated with both reduced native and increased exotic vegetation
which can reduce the abundance of phytophagous insects
(Burghardt et al. 2010; Narango et al. 2017). These changes
in vegetation, in turn, could have a significant effect on birds,
such as chickadees, if they rely on these insects and

Urban Ecosyst (2019) 22:1113–1122

caterpillars to feed their nestlings. Though much attention
has been paid to the effects of climate change on breeding
phenology, less study has been dedicated to understanding
how land use change and urbanization may influence phenological patterns. Increased temperatures in urban areas have
been associated with advanced leafing and flowering phenology in spring blooming plants (Luo et al. 2007; Neil and Wu
2006; White et al. 2002) which could potentially advance
insect emergence (Forrest 2016; Nilsson and Källander
2006). Therefore, some bird species that rely on insect abundance to time their reproduction may be unable to adjust their
breeding timing to match peak food availability in urban areas
and suffer reduced reproductive success. However, few studies have directly investigated how prey availability varies
along an urban-rural gradient and whether this could lead to
phenologic mis-match. A meta-analysis on passerine birds
found general patterns of earlier nesting, smaller clutch size,
lower nestling mass, and lower fledging success in urban populations; however, this pattern of lowered reproductive success of birds occupying urban landscapes was not universal
(Chamberlain et al. 2009) For instance, a wide scale study
across Europe, North Africa and the Middle East found clutch
size in migratory collared flycatchers (Ficedula albicollis),
and pied flycatchers (Ficedula hypoleuca) decreased as degree of urbanization increased, but urbanization was not related to clutch size in resident blue tits or great tits (Vaugoyeau
et al. 2016). Perhaps the ability to adjust reproductive phenology to local timing of prey emergence allows some urban
populations to adapt.
Whether urbanization has a positive, negative or neutral effect
may depend on both the bird species in question and the degree
of urbanization. For instance, some urban dweller species such as
house sparrows (Passer domesticus) thrive in urban areas
(Fischer et al. 2015). These species are found in high densities
even in heavily urbanized areas and often depend on anthropogenic resources (Seress and Liker 2015). Some species, termed
urban avoiders (Blair 1996; Fischer et al. 2015), do not fare as
well in urban environments; they are found in very low densities
in cities as they tend to be habitat specialists who require certain
features absent from urban environments (Seress and Liker
2015). Other species, such as mountain chickadees (Poecile
gambeli; Marini et al. 2017a) are urban utilizers (Fischer et al.
2015) and are able to adapt to intermediate levels of urbanization,
often taking advantage of food sources, nesting boxes or other
resources found in suburban habitats (Seress and Liker 2015).
However, some urban utilizer birds lay smaller clutches in the
city (Wawrzyniak et al. 2015; Glądalski et al. 2017) suggesting
that some urban habitats are lower quality than native woodlands.
Mountain chickadees are found year-round in mountainous
regions of western Northern America. Though they naturally nest
in secondary cavities found in coniferous forests, they will readily nest in artificial nest boxes and invade the edges of urban
environments. Research on neighboring urban and rural

Urban Ecosyst (2019) 22:1113–1122

populations in interior British Columbia found no difference in
reproductive success between the two habitat types, but nestling
feathers grew faster in urban environments, which may suggest
better nestling condition (Marini et al. 2017a). Another study
found males in urban habitat had greater song output in the early
breeding season than rural males, possibly because urban mountain chickadees may have better winter food resources (bird
feeders) than rural birds (Marini et al. 2017b). Urban mountain
chickadees bred significantly earlier than their rural counterparts,
but there was no evidence that urban mountain chickadees suffer
reduced reproductive success (Marini et al. 2017a). This finding
suggests that despite the differences between urban and natural
habitat, urban mountain chickadees may still time their reproductive cycles to coincide with peak caterpillar availability; urban
birds may breed earlier in the city because warmer temperatures
and non-native vegetation may advance peak timing of caterpillar abundance, and the birds correspondingly adjust their reproductive timing. However, it is also possible that mountain chickadee’s reproductive cycles are no longer synced to caterpillar
abundance in urban habitat, but their reproductive success is
not reduced due to alternate food sources available for feeding
young.
Because previous studies documented an advance in the
nesting of urban birds, but did not have a causal mechanism
to explain this change, the purpose of this study was to determine the relationship between caterpillar phenology and breeding timing in urban and rural chickadee populations. We hypothesize that the higher temperatures in urban landscapes may
alter vegetative phenology, and thus the timing of prey availability relative to rural areas. We predict that peak caterpillar
abundance (assessed via measuring frass mass) will be earlier
in urban habitats and that differences timing of nest initiation
across habitats corresponds with peak caterpillar abundance.
We also hypothesize that local prey availability around nests
should influence reproductive success rates. As most parental
feeding trips target trees close to the nest site, with the majority
of birds preferring to forage within approximately 20-30 m
from the nest (Stauss et al. 2005; García-Navas and Sanz
2011), we predict that vegetative species and cover near the
nest influence caterpillar phenology and abundance, and this
may in turn predict differential fledging success.

Methods
Field methods
Field work was conducted in Kamloops, BC, Canada
(50°40.23′ N, 120°23.86′ W) during the 2017 breeding season
(May to July). We monitored 144 nest boxes across rural and
urban habitat in south Kamloops. Our rural location is located
within Kenna Cartwright nature park, a relatively undisturbed
800 ha wilderness area only accessible by walking trails and a

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single maintenance road – chickadees have access to 66 nest
boxes erected in the central 80 ha of the park where native
sage-brush grassland transitions to coniferous forests (see
Marini et al. 2017a Fig. 1). The vegetation in this subsection
of the park represents a mosaic of mature coniferous forest
dominated by ponderosa pine (Pinus ponderosa) and
Douglas fir (Pseudotsuga menziesii), and is surrounded by
grassland ecosystems consisting mainly of bunchgrass
(Pseudoroegneria spicata) or sagebrush (Artemisia
tridentata). Deciduous canopy (with the exception of scarcely
occurring trembling aspen (Populus tremuloides)), is largely
limited to sub-canopy shrubs including saskatoon,
(Amelanchier alnifolia), chokecherry (Prunus virginiana),
and Douglas maple (Acer glabrum). Our urban location included 78 nest boxes distributed across sites ranging from
suburban backyards, open parks neighboring dense housing
areas to the Thompson Rivers University campus. Urban vegetation around Kamloops is generally highly variable, and in
comparison with native vegetation, has many more non-native, deciduous trees and shrubs (e.g., maple, fruit trees etc.)
mixed in with native conifers and shrubs. Previous research
conducted in these two study sites found our rural areas had a
greater canopy cover (65%) compared to urban areas (18%),
but that our urban areas have a greater percent of that canopy
cover comprised of deciduous vegetation (33%) compared to
our rural area (0.08%; Marini et al. 2017b).
In early May, we checked all nest boxes weekly for signs of
nesting (excavation of pine shavings, fur lined bottom). If nest
boxes appeared to be active, we continued to check them
every one to three days. If nests appeared inactive they were
checked every one to two weeks to ensure they did not later
become active. We collected data from each active nest to
determine the date of first egg, clutch size, hatch date, number
of eggs hatched, fledge date and number of offspring successfully fledged. To prevent premature fledging, we stopped
checking the nests 3 days before the expected fledge date
(around 15–18 days after hatch date). The number of young
successfully fledged was determined by counting the number
of young observed at the last box check and then subtracting
the number of dead nestlings, if any, found in the box after the
fledge date. Overall, 95 nestlings from 16 broods were monitored over the course of the study.
We monitored the frass levels around all rural and urban
boxes with nests started by chickadees. We also paired each
active nest to a nearby inactive nest box (approximately 200 m
away) in order to control for the effect of predation by mountain chickadees on frass collected and to examine potential
differences in food availability between active and inactive
nest boxes. One active nest box was not located within
200 m of any inactive boxes so no frass samples were included
from this location. In total, frass was collected at 12 rural nest
boxes (6 active and 6 inactive boxes) and 18 urban nest boxes
(9 active and 9 inactive boxes).

Urban Ecosyst (2019) 22:1113–1122

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Fig. 1 Series of photos demonstrating the construction (a, b, c) and set up (d) of our frass traps. Note that the actual frass traps used did not have the
bucket handle upwards like image D, and contained a pebble in the center of the bucket

Frass collection
To estimate caterpillar abundance, we used a variation of the
frass-fall method used in many previous studies (Liebhold and
Elkinton 1998; Tinbergen and Dietz 1994; Van Balen 1973) to
capture frass (caterpillar excrement) as it fell from the tree
canopy. We constructed traps to collect frass by taking large
plastic buckets (diameter 24 or 30 cm), and drilling holes in
the bottom to allow rain water to drain (Fig. 1). We also placed
3 to 4 heavy rocks into each bucket to prevent the buckets
from being knocked over by wind. Then we taped a square of
screen door mesh over the opening of each bucket to create a
shallow concave indent on which we placed a napkin to collect the frass. To hold the napkin in place we placed an elastic
band around the diameter of the bucket.
Because predation by mountain chickadees may have an
impact on the abundance of caterpillars, we paired each active
nest we surveyed with an inactive (not used for nesting) nest
box located approximately 100-200 m away to determine
whether frass mass differed between active and inactive nest
sites. At each study location, we set out one frass trap at an
active nest and another at its inactive pair on the same day
sometime between May 16 and May 29. We placed the traps
north of the nest box under any vegetative canopy at least 2 m
high and located approximately 10 m away from the nest box.
We then recorded the time we set the trap out, the woody plant
species above each trap, and classified each species by growth
form (tree or shrub) and leaf type (deciduous or coniferous).
After three days, we collected the frass at both the active and
inactive nest locations. We recorded the time the napkin was
removed, and then we placed each napkin in a labelled paper
bag for transport and storage in the lab. Next, we moved the
frass trap clockwise 90° around the nest box under a new tree
and placed a new napkin on the trap. Again, we left the traps
out for 3 days. We repeated this cycle throughout the breeding
season until fledging occurred at the active nests (late June/
early July), resulting in sampling each of the four cardinal
directions several times to give us an average of frass-fall in
the vegetation surrounding individual’s nests. We chose to

rotate the frass trap around our nest site instead of leaving it
deployed in one location to account for potential variation in
the availability of caterpillars on the vegetation in the immediate vicinity of the nest where adult birds are most likely to
make foraging visits. This approach also guards against inadvertent selection of a particularly productive or nonproductive frass site, and thus mis-representing the potential
resource to which the parents have access. It is important to
note the frassfall method does have limitations and is prone to
variation due to many factors such as temperature and rainfall
(Zandt 1994). However, since we used the same criteria to
choose trap locations at every site this should allow us to
compare frass mass and phenological changes between our
urban and rural sites.

Vegetation surveys
We surveyed vegetation cover at each active nest box location
and its paired inactive nest box by using measuring tapes to
establish a 17 m by 40 m plot using the nest box location as the
center of the plot. This plot size is typical of an average house
lot in Kamloops and was conducted as part of a concurrent
study (LB; unpublished data); several urban nest sites were
contained within private backyards where we could not survey
the vegetation outside of the property boundary, so this plot
size was used to keep measurements consistent at each site.
Within this plot we identified each species of tree and shrub
present, and estimated the percent cover of each. We chose to
calculate percent cover as this gives us an estimate the amount
of foliage available for foraging by mountain chickadees.

Frass measurements
The frass samples collected from the field were stored in the
lab for several weeks before analysis. We used paintbrushes to
brush the frass off of each napkin into a tin dish and removed
obvious vegetation and other contaminants from the samples
using tweezers. We then dried the samples in an oven at 38–
41 °C for 48 h. Next, we examined the samples under a

Urban Ecosyst (2019) 22:1113–1122

dissecting scope, removed any remaining debris, and then
weighed the samples on an analytical balance. To remove
the effects of varying surface areas of the buckets and duration
the traps were set out, for each sample collected we calculated
the amount of frass (in μg) per hour per cm2 of the trap surface. Some frass samples were contaminated with significant
amounts of dust which skewed the mass of the samples; therefore, we eliminated 23 samples that were visibly dusty from
future analysis.

Statistical analysis
We first asked whether timing of breeding (first-egg date)
differed between habitats by performing a Wilcoxin signedrank test. To ask whether frass mass changed throughout the
breeding season and varied across habitats, we constructed a
linear mixed model with the ln (frass mass) as the dependent
variable, and the Julian date of collection, habitat type (urban
or rural) and their interaction as model effects. To make direct
comparisons with the timing of chickadee reproduction, we
constructed a second model with all the same parameters except instead of Julian date, day of frass collection relative to
hatch date was included as a main effect. Interaction terms
with a P > 0.1 were removed and models rerun. We used an
alpha value of 0.05 to determine model significance. All frass
samples from paired active and inactive nests were included in
this model, so the name of the pair location was included as a
random effect because active and inactive paired boxes were
spatially coupled (within 200 m).
To determine whether the peak of maximum frass mass
differed in timing across habitats, we constructed another linear mixed model with the Julian date of maximum frass mass
as the dependent variable, habitat type as the model effect and
the name of the pair location of each nest as a random effect.
We constructed another model with the same parameters except the day of maximum frass mass relative to hatch date was
substituted for the Julian date of maximum frass mass.
We constructed three additional linear mixed models to
determine if frass mass varied with habitat type or vegetative
cover. The dependent variables were average mass of frass
pre-hatch date, average mass of frass post-hatch date and average mass of frass throughout the breeding season respectively, and the model effects were habitat type, deciduous percent
cover, coniferous percent cover and flower percent cover for
each model. The name of the pair location of each nest was
included as a random effect. We then conducted a backward
stepwise removal of non-significant terms.
To determine whether frass mass and timing were related to
fledging success, we used a generalized linear model with
Poisson error distribution and log link function. The number
of offspring fledged was used as the dependent variable and
habitat type, average mass of frass post-hatch date, average

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mass of frass pre-hatch date, day of maximum frass and Julian
date of maximum frass as model effects.
We conducted paired t-tests to ask whether frass mass differed between active nests and their neighboring inactive
nests. Specifically, we examined: average mass of frass prehatch date, average mass of frass post-hatch date, average
frass mass throughout entire breeding season, day of maximum frass relative to hatch day, Julian date of maximum frass,
and the mass of the maximum frass sample.
To determine if the species or type of vegetation (deciduous
tree, coniferous tree, deciduous shrub, or coniferous shrub)
above each frass trap influenced frass mass, we constructed
a linear mixed model with ln (frass mass) of each sample as
the dependent variable, vegetation type above each sample,
habitat type and Julian date as the model effects, and name of
the location of each pair as a random effect.
All statistical analyses were conducted in JMP 14.0 (SAS
Institute Inc. 2018); figures were created in R 3.4.3 (R Core
Team 2017) using the ggplot2 package (Wickham 2009).

Results
Consistent with previous studies (Marini et al. 2017a), chickadees initiated nesting approximately one week earlier in urban habitats (n = 9 nests) with a mean first egg date of May 4
± 5.2 days, compared to rural habitat (n = 6 nests) with a mean
first egg date of May 11 ± 3.1 days (z = 2.61, p = 0.009). The
amount of frass collected increased over the duration of our
study in both urban and rural environments (date: F1,13.5 = 5.8,
p = 0.03; habitat: F1,175.4 = 33.07, p < 0.0001; Fig. 2). When
we examined frass in relation to hatch day (hatch day = 0), we
detected a significant relationship, with frass increasing over
time (F1,179.9 = 34.7, p < 0.0001) and an additional effect of
habitat (F 1,13.0 = 13.91, p = 0.003), indicating a greater
amount of frass in rural habitat (Fig. 3).
The average date on which we recorded the maximum
mass of frass was significantly earlier in urban habitat
(June 3 ± 1.4 days) compared to rural habitat (June 10 ±
1.8 days; F1,13 = 6.32, p = 0.03; Fig. 4). However, when we
examined the day we recorded the maximum amount of frass
relative to hatch date, there was no significant difference between urban habitat (11.9 ± 5.2) and rural habitat (11.4 ± 6.2;
F1,13 = 0.05, p = 0.82; Fig. 4).
We found no effect of vegetative percent cover (coniferous,
deciduous and flower cover) on frass mass in any of the
models, so these effects were removed from subsequent
models. However, frass mass was higher in rural habitat than
urban habitat when we examined the average frass mass
throughout the entire breeding season (F1,13 = 10.34, p =
0.007). We then split the data to examine frass during the
pre-hatch and post-hatch period; frass mass during the prehatch period did not differ between habitats (F1,13 = 7.07,

Urban Ecosyst (2019) 22:1113–1122

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maximum frass collection, day relative to hatch date of maximum frass collection and the mass of the maximum frass
sample (Table 1).
Finally, we asked whether the type of vegetation located
above each frass trap had an impact on the mass of the sample
collected (n = 183 frass samples). However, vegetative type
(coniferous tree, deciduous tree, coniferous shrub or deciduous shrub) did not predict amount of frass collected (F3,173.2 =
0.59, p = 0.62). As expected, both habitat type (F1,14.97 = 6.17,
p = 0.03) and Julian date (F1,172.7 = 32.36, p < 0.0001) predicted ln(frass mass).

Discussion

Fig. 2 Scatterplot with lines of best fit (and SE) illustrating the change in
frass mass in relation to Julian date in urban (gray) and rural (black)
habitat over the breeding season

p = 0.09), though post-hatch frass mass was significantly high
in rural habitat (F1,13 = 7.23, p = 0.02). Ultimately, however,
we found no effects of habitat type, frass mass, or timing of
maximum frass on the number of young fledged (all p > 0.54).
In addition, we found no differences between active and inactive nests with respect to frass mass (pre-hatch date, post-hatch
date and throughout whole breeding season), Julian date of

Fig. 3 Scatterplot with lines of best fit (and SE) illustrating the change in
frass mass in relation to day relative to hatch day (hatch day = 0) in urban
(gray) and rural (black) habitat over the breeding season

Similar to previous studies on this population (Marini et al.
2017a), we found that urban mountain chickadees initiated
nesting approximately one week earlier than birds in rural
habitat. As expected, frass mass increased over the breeding
season, but the timing of peak frass mass occurred approximately one week earlier in urban environments, supporting
our predictions that early breeding timing in urban birds
may correspond to the earlier insect emergence occurring in
the city. Consistent with this idea, in both urban and rural
environments, peak frass mass occurred approximately
11 days after hatching coinciding with peak nestling food
demand. In the post-hatch period, we found that rural habitats
had higher frass abundance than urban sites, but despite this
we found no evidence of reduced reproductive success in urban birds compared to rural populations. Taken together, the
shifted timing of nesting and similar fledging success suggest
that urban mountain chickadees may have advanced their reproductive cycles to correspond to earlier peak abundance of
caterpillars found in an urban environment.
Earlier nesting in urban habitat is a trend found among
many bird species (reviewed in Chamberlain et al. 2009),
including species related to mountain chickadees such as great
tits (Wawrzyniak et al. 2015), and blue tits (Glądalski et al.
2015). One potential reason for earlier breeding in cities is the
presence of artificial food resources such as bird feeders available throughout the winter season. In their natural environment, some chickadee species rely on winter food caches
(Sherry 1984), but the stability of urban food resources may
allow females to maintain a higher overwinter mass and reach
egg condition earlier than rural birds. Correspondingly, birds
with access to supplemental food resources tend to breed earlier (reviewed in Robb et al. 2008). However, problems can
arise if anthropogenic food resources shift reproductive timing
so much that birds are no longer in synchrony with natural
food sources; anthropogenic food sources drive earlier breeding in urban Florida scrub jays (Aphelocoma caerulescens),
but evidence suggests these birds have reduced reproductive
success possibly because their reproductive cycle is no longer

Urban Ecosyst (2019) 22:1113–1122

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Fig. 4 Relationship between
habitat type and Julian date of
maximum frass mass (left) and
day of maximum frass mass relative to hatch date (right). Julian
date of maximum frass collection
was significantly earlier in urban
habitat; however, there was no
difference in the day of maximum
frass relative to hatch date between urban and rural
environments

in sync with insect abundance (Schoech and Bowman 2001).
However, this does not appear to the case for mountain chickadees, as we found no evidence of reduced reproductive success in urban environments. Urban birds still appear to sync
their reproductive cycles with local caterpillar abundance so
that the day of maximum frassfall occurs at 11 days after
hatching in both urban and rural habitats.
There are several mechanisms that could lead to earlier
peak caterpillar abundance in urban environments. Urban
areas are often associated with warmer temperatures due to
the heat island effect (reviewed in Rizwan et al. 2008); this
phenomenon is largely thought to be due to human activities
that produce heat (such as driving) and the presence of urban
buildings, which absorb and re-emit solar radiation. Warmer
temperatures advance the bud burst of trees and the rate of
caterpillar development (Buse et al. 1999), resulting in an
earlier caterpillar abundance peak (Kearney et al. 2010;
Smith et al. 2011). Correspondingly, birds tend to nest earlier
during warmer springs (Van Balen 1973; Kruk et al. 1996;
Glądalski et al. 2015). It may be beneficial for future studies
to record the temperature at urban and rural nesting locations
to confirm if warmer urban temperatures are advancing caterpillar phenology. Additionally, differences in vegetation may
account for the advanced caterpillar phenology in urban habitat, as timing of caterpillar peak abundance has been shown to
Table 1 Results of the paired ttest run on frass data variables
collected from paired active and
inactive nest locations

depend on tree species (Blondel et al. 1992; Sisask et al. 2010;
Veen et al. 2010). Despite not finding vegetation type to affect
measures of frass mass in this study, our urban study sites do
have a higher percentage of deciduous vegetation than our
rural study sites, and deciduous tree species tend to have an
earlier (Blondel et al. 1992; Tremblay et al. 2003) and shorter
peak caterpillar abundance than coniferous trees (Veen et al.
2010). Urban areas are also associated with increased nonnative vegetation (reviewed in McKinney 2002) which may
lead to differences in timing of bud burst and caterpillar biomass between urban and rural habitats.
Contrary to our results, a study in Hungary found urban
peak caterpillar biomass was not significantly earlier than rural habitat even though leaf emergence did occur earlier in
urban habitats (Seress et al. 2018). Instead, urban areas
showed several small peaks in abundance while only the forest sites show the expected single peak in frass abundance.
This suggests the pattern of earlier urban peak caterpillar biomass is not universal and may vary depending on local factors
such as degree of urbanization, and type of vegetation and
lepidopteran species present.
Though the peak date of frass mass was one week earlier in
urban habitat, peak frass mass in both habitats occurred when
nestlings were approximately 11 days old. This timing is consistent with peak food demand in other members of the

Variable

Mean Inactive

Mean Active

t

p

n

Mass frass pre-hatch date

0.04(0.01)

0.03(0.01)

0.91

0.39

8

Mass frass post-hatch date

0.09(0.01)

0.09(0.01)

0.44

0.67

15

Mass frass whole breeding season

0.08(0.01)

0.08(0.01)

0.30

0.76

15

Day of max frass

12.1(1.3)

11.1(1.7)

0.45

0.66

15

Julian date of max frass

157.3(1.3)

156.5(2.1)

0.41

0.69

15

Maximum frass mass

0.17(0.03)

0.16(0.02)

0.50

0.63

15

Active and inactive nest locations did not differ significantly in terms of average mass (SE in parentheses) of frass
collected pre-hatch date, post hatch-date and throughout the entire breeding season, day relative to hatch date of
maximum frass collection, Julian date of maximum frass collection or the mass of the maximum frass samples collected

1120

Paridae family; great tit and blue tit nestlings have the highest
food demands around 10–11 days after hatch date (Perrins
1965). Thus, in natural environments these birds synchronize
their breeding cycles so that peak caterpillar abundance also
occurs at this time (Blondel et al. 1999; Naef-Daenzer and
Keller 1999; Charmantier et al. 2008). However, though our
study suggests birds time their breeding to correspond with
peak frass mass in both urban and rural habitat, other studies
on tits in Europe have found conflicting results. For instance,
only urban populations of great tits in Poland timed reproduction in relation to peak caterpillar abundance; no relationship
was found in rural populations. However, this lack of relationship may be a result of the high density of caterpillars found in
the rural forest throughout the entire breeding season making
it unnecessary for birds in this habitat to closely track the peak
abundance of caterpillars (Wawrzyniak et al. 2015).
Overall frass mass was significantly higher in our rural study
site, a pattern also observed in several studies of tits in urban and
rural environments (Marciniak et al. 2007; Glądalski et al. 2015;
Pollock et al. 2017; Seress et al. 2018). This pattern may be due
to the higher canopy cover in our rural study site as well as the
presence of exotic vegetation in our urban study site. Native plant
species often support a higher abundance and diversity of native
caterpillars than non-native vegetation (Burghardt et al. 2010;
Narango et al. 2017). Our study found no influence of vegetation
type on frass mass; however, we did not examine the differences
between native and non-native vegetation specifically, which
may be an interesting area for future research. An important
factor in our study that differs from related studies on European
tits (Glądalski et al. 2015; Pollock et al. 2017; Seress et al. 2018),
is that differences in frass mass were not associated with differences in reproductive success between urban and rural habitats.
One explanation may be the presence of different caterpillar species in the two habitats. Caterpillar species utilized by birds differ
in size (Naef-Daenzer and Keller 1999; Nour et al. 1998), detectability (Lichter-Marck et al. 2015) and carotenoid content
(Arnold et al. 2010). Therefore, more nutritious species may
reside in cities so that despite the lower frass mass in those areas,
urban birds do not suffer reduced reproductive success. For example, García-Navas and Sanz (2011) found that blue tits preferred certain caterpillar types and that nest visitations declined
and nestling condition increased as birds fed a higher ratio of
preferred caterpillars to their young. Nutritional quality appears
to play an important role in caterpillar selection as some of the
most abundant caterpillars in this study were not proportionally
fed to blue tit nestlings. Therefore, it is important to consider that
the frass mass we have collected may not necessarily reflect the
caterpillars the mountain chickadees are utilizing and this study
would benefit from future research identifying which caterpillars
are brought to chickadee nests and assessing whether frassfall
collected reflects the abundance of these species. We also did
not directly measure the abundance of caterpillars in our habitat
and instead only measured the mass of frass collected from point

Urban Ecosyst (2019) 22:1113–1122

locations below the canopy. In the future it may be beneficial to
use direct counts of caterpillars on tree branches (Visser et al.
2006) to see if frass mass in rural habitat truly relates to a higher
caterpillar abundance.
Consistent with previous studies on this population, our
results suggest that mountain chickadees have acclimated well
to urban living (Marini et al. 2017a; Marini et al. 2017b); these
birds appear to be breeding earlier to correspond with earlier
food abundance in the city, and we found no impact of urbanization on fledging success. Closely related black-capped
chickadees (Poecile atricapillus), though found in lower densities in the city, also appear to have no significant difference
in reproductive success in urban and rural habitats (Blewett
and Marzluff 2005). However, a number of studies done on
tits, relatives of the chickadees in Europe, show that not all
populations are as successful; often urban broods of great tits
and blue tits suffer reduced reproductive success in urban
environments (Glądalski et al. 2015; Wawrzyniak et al.
2015; Glądalski et al. 2017; Preiszner et al. 2017). These conflicting findings may be due to differences in the degree of
urbanization between study sites, species-specific differences
in adaptations to urban environments, or site-specific factors.
Surprisingly, we found no relationship between fledging
success and frass mass in either of our habitats, suggesting
that chickadees may rely on food sources other than caterpillars or that the frass we have collected may not reflect caterpillar species utilized by chickadees. However, it is important
to consider our study has a small sample size (n = 16 broods)
and includes only one year of data (2017) so further study for
repeatability of these patterns in other years is warranted.
Overall, our study highlights the importance of precise reproductive timing to nestling food availability. Urban mountain chickadees appear to have acclimated well to urbanization
by advancing their reproductive timing to correspond to earlier food abundance in an urban environment. Unlike similar
studies on tits in Europe (Marciniak et al. 2007; Gladalski
et al. 2015; Wawrzyniak et al. 2015), urbanization has not
reduced reproductive success of mountain chickadees in the
city. Thus, mountain chickadees appear to be able to respond
to changes in resource availability which may allowing urban
birds to successfully produce offspring in an environment very
different from their natural habitat.
Acknowledgements The authors thank Aneka Battel, Chelsea Reith
and the many volunteers who helped in the field. Thank you also
to the associate editor and two anonymous reviewers whose comments improved the quality of the manuscript. Funding was provided by the Natural Sciences and Engineering Research Council
of Canada through an Undergraduate Student Research Award
(ACH) and Discovery Grants to MWR and KAO. The authors
would like to acknowledge that our work was conducted on
unceded First Nations land (Tk’emlúps te Secwépemc and
Skeetchestn First Nations) and also thank the City of Kamloops
and homeowners in Kamloops for access to parks and backyards.

Urban Ecosyst (2019) 22:1113–1122

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