AVIAN NEST PARASITES AND PARENTAL FEEDING BEHAVIOUR IN URBAN AND
RURAL MOUNTAIN CHICKADEES
by
Alexandra Rae Lamberton
BSc Biology, Vancouver Island University 2017

THESIS SUBMITTED IN PARTIAL FULFILLMENT OF
THE REQUIREMENTS FOR THE DEGREE OF
MASTERS OF SCIENCE
IN
NATURAL RESOURCES AND ENVIRONMENTAL STUDIES - BIOLOGY

UNIVERSITY OF NORTHERN BRITISH COLUMBIA
April 2024
© Alexandra Lamberton, 2024

ABSTRACT
Urbanization is considered one of the greatest human-caused threats to biodiversity. Human
development and encroachment on native habitats and its impacts on species, however, is
nuanced; while it has been found to create detrimental impacts on some species, certain aspects
of urbanization may benefit others. This interaction of advantages vs constraints offered by
urban landscapes is especially relevant to species that show sufficient behavioural plasticity to
settle in this rural/urban interface. The objective of this thesis is to investigate some of these
potential costs/benefits of urbanization in mountain chickadees. I first assess a potential positive
effect of urban settlement noted in other systems – a decrease in the incidence of nest
ecotparasites found in urban landscapes - in mountain chickadees nesting in Kamloops, BC,
Canada. I enumerated the blowflies and fleas found in collected nests in 2019 and 2020 to
determine whether nest parasitism differs between urban and rural habitats in the region, and
whether this in turn influences nest success (Chapter 2). I found that abundance of blow fly
puparia was higher in rural nests, but that flea abundance was associated with temperature and
not urbanization. Additionally, I observed that urban nests fledged approximately one additional
chick per nest. This suggests urban habitats could lift some constraints that would normally
decrease nestling condition. I then compared rates of adult chickadees feeding nestlings to
determine whether differences in ectoparasitism levels between habitats results in compensatory
feeding by parents, and if this affected the growth rate of nestlings (Chapter 3). I did not find
evidence that urbanization or ectoparasite abundance influenced parental feeding or growth rate.
I did find that feeding rate was lower and that growth rate was higher in warmer years. Other
studies showing potential differences in prey availability between habitats, with rural sites
having potentially greater abundance of prey, may help explain my results – while prey might be

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more abundant in one habitat, nestling condition may be less affected by parasite infestation in
the other, helping balance the costs/benefits of settlement between habitats. While my results
provide some evidence that reduction of parasites in urban areas can benefit urban settling
species, further research will be required to determine the mechanism that causes this
phenomenon.

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Preface
Funding for this research was provided through Natural Sciences and Engineering Research
Council of Canada (NSERC) Discovery Grants to M.W.R. and K.A.O., and by the University of
Northern British Columbia through a Graduate Entrance Scholarship, a Graduate Entrance
Research Award. All work was approved by the University of Northern British Columbia
Animal Care and Use Committee (UNBC-2017-01 and UNBC-2020-01) and was conducted
under a Canadian Federal Master Banding Permit and Scientific Collection Permit no. 10940.
The design, execution, and analysis of all experiments in this thesis were directed by A. R
Lamberton, thus the thesis is written in first person singular. However, I would like to
acknowledge the significant contribution of collaborators throughout the entirety of
this Master of Science degree.

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Table of Contents
ABSTRACT ................................................................................................................................... ii
Preface ........................................................................................................................................... iv
List of Figures ............................................................................................................................. viii
Acknowledgements ...................................................................................................................... ix
CHAPTER 1:

GENERAL INTRODUCTION. ........................................................................1

1.1 Urban ecology and birds ..................................................................................................... 1
1.2 Study species ....................................................................................................................... 3
1.3 Ectoparasitism ..................................................................................................................... 5
1.4 Parental care ........................................................................................................................ 7
1.5 Study site ............................................................................................................................. 9
1.6 Field methods .................................................................................................................... 11
1.7 Habitat Classification ........................................................................................................ 12
1.8 Thesis Overview ............................................................................................................... 14
1.9 References ......................................................................................................................... 15
CHAPTER 2: BLOWFLY AND FLEA INFESTATION OF MOUNTAIN
CHICKADEE NESTS .................................................................................................................21
2.1 Introduction ....................................................................................................................... 21
2.2 Methods............................................................................................................................. 25
2.2.1 Nest location and monitoring ................................................................................... 25
2.2.2 Nest collection ......................................................................................................... 26
2.2.3 Parasite identification............................................................................................... 27
2.2.4 Statistical analysis .................................................................................................... 28
2.3 Results ............................................................................................................................... 30
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2.3.1 Identifications .......................................................................................................... 30
2.3.2 Abundance of blow fly puparia relative to urbanization, ambient temperature, and
year. ................................................................................................................................... 30
2.3.3 Abundance of adult fleas relative to urbanization and year. .................................... 32
2.3.4 The effect of parasites and habitat type on number of chicks fledged..................... 34
2.4 Discussion ......................................................................................................................... 35
2.4.1 Blow flies ................................................................................................................. 36
2.4.2 Fleas ......................................................................................................................... 37
2.4.3 Nest success ............................................................................................................. 38
2.5 References ......................................................................................................................... 40
CHAPTER 3: PROVISIONING RATES OF MOUNTAIN CHICKADEES IN URBAN
AND RURAL HABITAT ............................................................................................................46
3.1 Introduction ....................................................................................................................... 46
3.2 Methods............................................................................................................................. 49
3.2.1 Video recording ....................................................................................................... 49
3.2.2 Data consolidation ................................................................................................... 51
3.2.3 Video analysis .......................................................................................................... 51
3.2.4 Frass collection ........................................................................................................ 51
3.2.5 Data analysis ............................................................................................................ 52
3.3 Results ............................................................................................................................... 54
3.3.1 Identity of food items ............................................................................................... 55
3.3.2 Temperature ............................................................................................................. 55
3.3.3 Parasite and nest box temperature............................................................................ 55
3.4 Discussion ......................................................................................................................... 59
3.5 References ......................................................................................................................... 63
CHAPTER 4:

CONCLUSIONS AND FUTURE DIRECTIONS .........................................67

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4.1 Nest parasitism and compensatory behaviour in mountain chickadee nests. ................... 67
4.2 Future Directions .............................................................................................................. 69
4.3 References ......................................................................................................................... 72

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List of Figures
Figure 1.1 Locations of mountain chickadee (Poecile gambeli) nest boxes in Kamloops, BC,
Canada. The majority of rural nest sites were located in Kenna Cartwright Park (A). Urban
sites were located at Thompson Rivers University campus (B) and in several urban
neighbourhoods throughout Kamloops (C). Photo credit; Google Earth pro. .............................. 11
Figure 1.2 Google Earth image of typical mountain chickadee (Poecile gambeli) nest sites
within the study site in Kamloops, BC, Canada. The left image shows a typical rural site and
the right shows a typical urban site. The blue circle has a radius of 75m and demonstrates the
approximate size of a mountain chickadee’s territory. Photo credit; Google Earth pro ............... 14
Figure 2.1 Boxplot comparing the maximum temperature during the nestling period during
2019 and 2020 comparing urban and rural environments ............................................................ 31
Figure 2.2 Boxplot the number of puparia found in nests during 2019 and 2020 comparing
urban and rural environments. ...................................................................................................... 32
Figure 2.3 Boxplot comparing the mean temperature during the incubation period during 2019
and 2020 comparing urban and rural environments. .................................................................... 33
Figure 2.4 Boxplot comparing the number of fleas found in nests during 2019 and 2020
comparing urban and rural environments. .................................................................................... 34
Figure 2.5 Boxplot comparing the number of chicks fledged in urban and rural environments. . 35
Figure 3.1 Image of an urban mountain chickadee nest box taken from a GoPro HERO7
camera. .......................................................................................................................................... 50
Figure 3.2 The feeding rate (trips/hour/chick) in both rural (grey) and urban (white) habitats
across the three years of the study. ............................................................................................... 56
Figure 3.3 The growth rate (mm/day) in both rural (grey) and urban (white) habitats across the
three years of the study. ................................................................................................................ 57
Figure 3.4 Temperature in Kamloops as recorded by a government weather station on the day
nest watch videos were taken compared. ...................................................................................... 58

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Acknowledgements
I would like to acknowledge this research was conducted on the traditional territory of the
Tk’emlúps te Secwépemc and analyzed and written on the traditional territory of the Lheidli
T’enneh First Nations. I would also like to thank the City of Kamloops for permitting me and my
fellow researchers to conduct research in Kenna Cartwright Park and the surrounding urban
green spaces and neighbourhoods.
I want to give a special thanks to my supervisors, Dr. Ken A. Otter and Dr. Matt W.
Reudink. I would never have been able to complete my research and writing without your
support, guidance, and patience. I would also like to thank my committee members Dr. Lisa
Porier for her help with designing my initial research and Dr. B Staffen Lindgren for his help in
refining my thesis to ensure I presented my best work.
I’d like to thank everyone who worked with me collect data and specimens during my
field work - Blaire Smith, Madison Oud, Cara Snell, and numerous volunteers from Thompson
Rivers University. Especially Madison Oud who collected nests for me in 2020 when I was
unable to go out in the field; I’m not sure I would have had enough samples without your hard
work.
I’d also like to thank my friends and family for all of their support throughout my degree.
Thank you to my parents for their support, for helping me move all the way up to Prince George,
and for taking care of the cats and all of the stuff I left in Ladysmith. Thank you to my Uncle
Dale and Aunt Cyndi their support, for helping introduce me to Prince George, and for driving
me around when I needed it. Finally thank you to my partner Colten Kennedy; you were
incredibly supportive while I analyzing my data and writing up my thesis, I don’t think I would
have been able to do this without you.

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CHAPTER 1: GENERAL INTRODUCTION.
1.1 Urban ecology and birds
As the human population surpasses 8 billion people, we’ve transformed the landscape in ways
that have had major consequences for natural populations (Chace and Walsh, 2004; Seto et al.,
2011; EPA, 2023). Urbanization is regarded as one of the most extreme forms of environmental
alteration as well as one of the largest threats to wildlife (Kurcuz et al., 2021; Isaksson and
Andersson, 2007). The percentage of humans living in urbanized environments is expected to
increase from 56% in 2022 to 68% in 2050, representing an increase in the global urban
population of an estimated 2 billion people (UN-Habitat, 2023). Given that urban expansion is
predicted to increase substantially over the next decades it is important to understand how some
animals adapt to urban environments, and whether this can provide insights into urban planning
to increase the diversity of organisms capable of living in the Anthropocene.
Urbanization is associated with a variety of environmental changes, many of which interact
in important ways to allow cohabitation of some species with humans. The microclimate of
urban areas often differs dramatically from neighbouring native habitat (Seress and Liker, 2015).
Urban areas are typically warmer than adjacent rural areas; a phenomenon commonly referred to
as the Heat Island effect (Hart and Sailor, 2009; Pickett et al., 2010). The Heat Island Effect can
be caused by the thermal and reflective properties of anthropogenic materials (concrete,
buildings etc), reduction in surface water availability, reduction in wind speed due to structures,
waste heat, and changes in vegetation all influence urban temperatures (Hart and Sailor, 2009;
Ryu and Baik, 2012). Reduction in tree canopy cover can elevate urban temperatures by both
increasing direct solar radiation to the ground and diminishing humidity levels (Hart and Sailor,
2009). The increased heat retention due to lower albedo of urban structures, decreased vegetation
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cover and more limited airflow in urban landscapes combine to elevate temperatures; this can
have negative consequences for animal settlement, but could also promote it in some cases.
Within cities, the reduced cover of native vegetation can result in a reduction in habitat for
both native birds and insects (Seress and Liker, 2015; Ruas et al., 2022). This shift in regional
habitat availability can be exacerbated by the planting of non-native species in gardens and
landscaped areas, the growth of which might be promoted by the warmer conditions in urban
areas (Ruas et al., 2022). This alteration of both temperature and vegetation may affect the
diversity and abundance of insect prey that form the primary diet of insectivorous birds (Seress
and Liker, 2015). Caterpillar biomass can be significantly lower in urban areas relative to rural
areas, though this effect is not ubiquitous, suggesting that urbanization effects may vary
geographically and with differences in the nature of both urban and native vegetation for the area
(Seress et al., 2018; Hajdaz et al., 2019; Kurcuz et al., 2021).
How birds respond to urbanization varies from species to species depending on how the life
history traits of individual species interact with the effects of urbanization (Blair, 1996). Blair
(1996) categorized bird species in urban areas as urban exploiters, urban adaptors, or urban
avoiders. Urban exploiters, like rock doves (Columbia livia), exploit urban habitats and reach
their highest population densities in urban areas (Blair, 1996). Urban avoiders, such as the
Hutton’s vireo (Vireo huttoni), are very sensitive to the habitat changes associated with
urbanization and therefore have significantly reduced population density in urban areas (Blair,
1996). Urban adaptors, such as the violet-green swallow (Tachycineta thalassina), are able to
exploit some aspects of urban habitats, but not to the degree urban exploiters do and have similar
population densities in urban and rural areas (Blair, 1996). While the category a species is in may
be location dependent, life history traits can be used to predict a species’ response to

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urbanization (Seress and Liker, 2015). Urban exploiters are often species that have had long
histories of occurring alongside humans and may even be dependent on human-provided
resources; examples include the house sparrow (Passer domesticus) and European starling
(Sturnus vulgaris) (Seress and Liker, 2015). Urban adaptors are typically species that are habitat
generalists able to colonize edge habitat, are often omnivorous, and may have nesting
requirements that can be adapted to vegetation or cavities available in cities. Their ability to take
advantage of human-supplied resources, such as food from bird feeders and nesting substrate
from ornamental vegetation or artificial nest cavities, allows these species to persist in urban
environments (Seress and Liker, 2015). Urban avoiders tend to consist of migratory species,
habitat specialists, and species such as ground nesters that are particularly susceptible to human
activity (Seress and Liker, 2015). Whether native species fall into the category of urban adapter
or urban avoider often depends on the interaction of their life history patterns and ecological
requirements, and how these are either met or negated by the specifics of the urban
environments. This thesis will investigate aspects of urban adaptability in the mountain
chickadee (Poecile gambeli).

1.2 Study species
Mountain chickadees are small, non-migratory songbirds that reside in the montane coniferous
forests of Western North America (McCallum et al., 2020). They are considered conifer
specialists due to their preference for nesting in conifer trees (McCallum et al., 2020). As with
many other members of the Paridae family (chickadees and titmice), the mountain chickadee is a
secondary cavity nester, using preexisting cavities in conifers as nest sites(McCallum et al.,
2020) and thus readily utilized artificial cavities such as nest boxes. In the breeding season adults
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and nestlings feed mostly on arthropods, and during the winter they rely on cached conifer seeds
(Grundel and Dahlsten, 1991; Kozlovsky et al., 2017; McCallum et al., 2020). When foraging for
arthropods, mountain chickadees almost exclusively utilize gleaning, where a bird, standing or
hanging from a branch, takes a stationary prey item from a tree or leaf (Cuadrao Gutiérrez, 1989;
McCallum et al., 2020). Because of mountain chickadees reliance on cached food and seeds in
winter, the availability of artificial bird feeders in urban environments may facilitate settlement
of chickadees during their typical juvenile dispersal period (first fall after hatching); the
availability of artificial nest sites (bird houses) may also promote breeding settlement. However,
if insect food availability is poor during the spring/summer months, then these urban ecosystems
may constitute ecological traps for this typically conifer-dependent species.
While habitat specialists like the mountain chickadee are typically predicted to be urban
avoiders, the mountain chickadee has a number of other life-history characteristics (cavity
nesting and omnivorous diet) that may allow sufficient behavioural flexibility to settle in urban
environments (Kozlovsky et al., 2017; Marini et al., 2017). During the winter, urban mountain
chickadees living in Reno, Nevada, USA, cached food at the same rate as rural mountain
chickadees, suggesting some degree of plasticity in foraging behavior (Kozlovsky et al., 2017).
Marini et al. (2017) observed that urbanization had no effect on clutch size, number of nestlings,
or the number of nestlings that fledged Kamloops, British Columbia, Canada. In some aspects
adults and nestlings seemed to do better in urban environments; feather growth rates were higher
in urban nests and adult urban females tended to be heavier than their rural counterparts. Nests
were also initiated significantly earlier at urban sites, which Marini et al. (2017) attributed to
improved overwinter condition of adults (likely due to availability of bird feeders) and warmer
microclimates in urban areas initiating earlier emergence of insect prey. Although Marini et al.

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(2017) found urban habitats had significantly reduced canopy area for foraging, the abundance of
deciduous trees in urban landscapes was far higher than native vegetation of the region. As
caterpillar larvae - the primary prey of chickadees - are often more abundant in deciduous than
coniferous vegetation (Hajdasz et al.,2019), this shift in vegetation structure might have helped
compensate for total reduced canopy volume in urban habitats.
Though urban and rural birds do not differ in reproductive success, they may still be exposed
to differing pressures associated with urban landscapes, such as predators (Smith et al., 2021),
anthropogenic hazards (e.g., cars, windows), and differences in nest parasite pressures. It is this
latter area that I will explore in this thesis, and the impact this has on parental behaviour of
mountain chickadees living in urban and rural landscapes.

1.3 Ectoparasitism
Though they are often overlooked, parasites are an important part of community ecology (Rocha
et al., 2016; Preston and Johnson, 2010). Parasitism is a widespread life strategy and parasites
can change host behavior, reduce host fitness, and reduce host abundance (Preston and Johnson,
2010; Frainer et al., 2018). The effect parasites have on ecosystems can be so significant that
some are considered keystone species (Preston and Johnson, 2010). Like their hosts, nest
parasites can be affected by changes in microclimate and other impacts of urban development
(Goodenough, et. al., 2011), and the interactions between hosts and parasites might vary between
urban and rural populations.
Ectoparasites are parasites that spend all or part of their lifecycle living on the body or in the
bedding of their hosts (Goater et al., 2014). Of particular interest to the study of nesting birds are
ectoparasites that live within the host’s nest material. The nest provides both a habitat and a
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nearby food source in the form of blood meals for nest ectoparasites, making it an ideal
environment for them (Heeb et al., 2000). As a result, cavity nesting birds and their young often
must deal with the negative consequences of nest ectoparasites, such as anemia and reduced
growth (Heeb et al., 2000).
Two of the most common types of ectoparasites in bird nests are fleas in the genus
Ceratophyllus and blow flies in the genus Protocalliphora (Heeb et al., 2000). Blow fly larvae
obtain blood meals from nestlings intermittently, returning to the nest material when full, and the
adults are free living and feed mostly on pollen(Roby et al., 1992; Wesolowski, 2001). Adult
fleas feed on both adults and nestlings and then shelter within the nest material when full(Tripet
and Richner, 1999). All life stages of fleas live within the nest box and adult fleas only leave the
nest box during dispersal on the bodies of adult birds (Tripet and Richner, 1999). Blood feeding
can have a range of effects on nestlings; from outright mortality to no noticeable effect (Loye
and Carroll, 1995; Musgrave et al., 2019). Blow flies can reduce growth rate of nestlings as well
as lower hematocrit levels (Hurtrez-Boussès et al.,1998; Harriman et al., 2014). Fleas can reduce
nestling body mass, wing and tarsus length, as well as the number of chicks fledged (Christe et
al., 1996; Heeb et al, 2000). However, other studies have observed no evident impact of blowfly
or flea parasitism on nestlings (Eva et al., 1994; Goodenough et al., 2011; Musgrave et al., 2019;
Castaño-Vázquez and Merino, 2021). Researchers have suggested that this lack of observable
effect may be due to behavioral compensation in the form of increased grooming or feeding by
parents (Tripet and Richner, 1997; Goodenough et al., 2011; Harriman et al., 2014).
Whether the effect of parasitism on nestlings is immediately apparent or is compensated for
behaviorally, the removal of parasites in the nest may increase nest success (O’Brien and
Dawson 2008). The parasite release hypothesis suggests that if parasites are reduced in urban

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areas their hosts may be more successful (Le Gros et al. 2011). Multiple studies have found that
urban habitats are associated with a reduced incidence of bird ectoparasites (Le Gros et. al.,
2011; Hamner et al., 2017). As high temperature can reduce the survival of both Protocalliphora
and fleas (Dawson et al., 2005, Castano-Vasquez et al., 2018), the elevated temperatures
frequently associated with urbanization (Pickett et al., 2011) could reduce ectoparasite
abundance. In addition, adult Protocalliphora are more abundant in areas with more vegetation
(Eeva and Klemola, 2013), something that is reduced under urbanization (Ruas et al., 2022). As
such, a reduction in ectoparasites in urban environments could help compensate for other
detrimental effects of urbanization on settling birds, and aid species in their plasticity to adjust to
anthropogenic landscapes.

1.4 Parental care
Parental care takes many forms in birds. Loosely it is defined as any parental trait or behavior
that enhances offspring fitness (Williams, 2018). More specifically, parental care in birds is
recognized as incubation of eggs, provisioning of food, grooming and sanitation, and providing
protection from weather and predators (Tripet et al., 2002, Mock 2022). During the nestling
stage, food provisioning is regarded as both the most important facet of parental care as well as
the most costly form of parental care to adults (Schwagmeyer and Mock, 2008).
In altricial species of birds, parents must provide food to nestlings and the rate at which they
are able to provide food determines growth rate, body condition, and fledging success (Williams,
2018). Parental provisioning is a major determinant of nestling success across a wide range of
bird species, including Parids (Schwagmeyer and Mock, 2008). High provisioning rates carry
high metabolic costs to parent birds and are known to decrease both survival and future
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reproductive success (Schwagmeyer and Mock, 2008). Provisioning young represents a trade-off
for parents; parents must feed their offspring enough for them to grow and then successfully
fledge, but they must balance the effort required for provisioning with the need to ensure their
own survival and future reproductive capabilities. Thus, anything that necessitates compensatory
feeding by the parents likely represents an increased cost to the parents.
Feeding rate depends on nestling age, food availably and quality, climate, and the number of
nestlings (Grundel, 1987; Koo Lee et al., 2011; García-Navas and Sanz, 2012). Factors like
blood loss from ectoparasites and adverse weather that increase the caloric needs of nestlings
may necessitate a compensatory increase in feeding rate by parents (Koo Lee et al.,2011; Tripet
and Richner, 1997; Harriman et al., 2014). As noted in section 1.1 and 1.3, urbanization can
modify weather, food availability, and levels of parasitism, suggesting that urbanization may
either reduce or enhance the need for compensatory feeding rates.
The effects of urbanization on feeding rate are somewhat mixed and likely location
dependent. Sinkovics et al., (2021) found an increase in feeding rate among urban great tits
(Parus major) coupled with a reduction in the quality of food delivered by parents. Urban and
rural young received the same amount of food, but urban parents fed their young more frequently
to compensate for poorer food quality (Sinkovics et al., 2021). However, in another study on
multiple bird species, Kurcuz et al., (2021) found no relationship between the level of
urbanization and the availability or quality of food or feeding rates of parents.
As mentioned in section 1.3, increased feeding may be a mechanism of compensating for
blood feeding by ectoparasites. Blue tit parents at nests infested with Protocalliphora increased
their provisioning rate by 29% in one study (Tripet and Richner, 1997). In another study of blue
tits, Hurtrez-Boussès et al. (1998) observed a 65% increase in feeding rate by parents at nests

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infested with Protocalliphora. Similarly Great tit parents increased feeding rate by 57% at nests
infested with hen fleas (Ceratophyllus gallinae).
Recent research on mountain chickadees by Bonderud et al. (2017) showed that feeding rate
did not differ between urban and rural birds, nor did it vary with the sex ratio of nestlings or the
number of trees around the nest box. Past studies on feeding rate and prey selection in mountain
chickadees have shown that feeding rate per nestling decreased with brood size but increased
with age (Grundel 1987) and that diversity of prey fell with increasing food demand (Grundel
1990). This suggests that mountain chickadees parents do adjust provisioning behavior with
demand to some degree, but not in all cases.

1.5 Study site
I conducted field work for this project in Kamloops, British Columbia, Canada 50.6745° N,
120.3273° W during the 2019 and 2020 breeding season and utilized additional data collected at
the study site in 2016 and 2018. Kamloops is located in the Thompson valley on the unceded
ancestral lands of the Secwépemc Nation. The study site I utilized is a nest box population
consisting of approximately 110 nest boxes distributed among a series of urban and rural subsites
across Kamloops. The site was established in 2013 and has been monitored on an annual basis
ever since. The nest boxes in both urban and rural sites were mounted 2 m off the ground on
mature trees with at least 75 m between boxes. Urban nest boxes were placed on Thompson
Rivers University (TRU) campus and residential areas in south Kamloops. Urban Kamloops
consists of some patchy natural grassland and forests as well non-native grasses and other plants
used for landscaping in residential and business areas. Rural nest boxes were placed in Kenna
Cartwright Nature Park, along the adjacent Copperhead Trail, and in green spaces interspersing
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urban neighbourhoods (ranging in size from 4 to 30 ha). The vegetation in Kenna Cartwright
Nature Park, the Copperhead Trail and retained greenspaces consists of mixed ponderosa pine
(Pinus ponderosa) and Douglas-fir (Pseudotsuga menziesii) forest, understory meadows, and
areas of shrubgrass at lower elevations. These areas have only minor human disturbance in the
form of walking trails. Kenna Cartwright Nature Park has a single, gated limited-access road for
park maintenance operations, but all the rural habitats used in this study are otherwise
representative of the natural ecological conditions for the region (Marini et al., 2017).
During the initial years of the project, various types of nest boxes were erected to determine
which would be used by settling birds. The majority of boxes erected have back and sides of
2cm thick cedar plank, with internal dimensions of approximately 10x10cm side to side and front
to back, and approximately 35cm top to bottom. The primary difference between box types was
the front, which varied using curved PVC, fir planks with attached bark, or cedar plank. All
boxes were standardized to be fronted with cedar planks in late summer of 2019, but a subset of
nest boxes sampled in 2019 were constructed with front made of PVC pipe (N=4) or constructed
with a front made of ponderosa pine bark (N=7). All other boxes in 2019 (N=12) were cedar
plank on front, back, sides and top/bottom; all nests used in 2020 (N=21) were of this
construction.

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Figure 1.1 Locations of mountain chickadee (Poecile gambeli) nest boxes in Kamloops, BC, Canada. The
majority of rural nest sites were located in Kenna Cartwright Park (A). Urban sites were located at
Thompson Rivers University campus (B) and in several urban neighbourhoods throughout Kamloops (C).
Photo credit; Google Earth pro.

1.6 Field methods
Beginning in mid-April of each field season, I checked each of the nest boxes every 1 to 6 days,
depending on the activity of the birds and what stage of nesting they were in. Once a nest start
was observed I checked active nests every 3 days to note the appearance of eggs and determine
the start of incubation (taken as the day of the last egg to appear in the clutch). After incubation
began, I checked nests every six days to avoid disturbing the female while incubating. I resumed
checking every two days starting on day 12 of incubation. To determine date of hatch, we
climbed to the nest box and carefully looked inside for hatched nestlings. After nestlings
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hatched, parents were banded on day 3 of the nestling cycle. Nestlings were banded and had
wing chord, leg length and mass measured on day 6, and I returned one final time (day 9) to
measure wing chord, leg length and mass again. Nests were then monitored by watching from a
distance for continued parental activity on day 15; any nests that were still active at day 15 were
considered to have reached successful fledging, as mountain chickadees typically fledge around
day 16, and disturbance to the nest tree after day 13-14 is likely to cause pre-mature fledging
(McCallum et. al., 2020, Gold and Dahlsten, 1983).

1.7 Habitat Classification
Most studies focusing on urbanization describe habitat in dichotomous terms, typically based on
the researcher’s judgement as to what constitutes each habitat type. To reduce subjectivity in how
boxes were placed, the original design of the study was to place these in areas that either had
very little human-made structures within 75m radius (the average foraging range of mountain
chickadees - McCallum et. al., 2020) or had significant anthropogenic structures in the same
radius. However, to quantitatively assess whether this created a clear distinction between
habitats, I calculated an Urbanization Index following LaZerte et al. (2017) and used this to
designated whether nest sites were urban or rural based on the index.
I utilized the protocols and scripts developed by LaZerte et al. (2017) to develop the
Urbanization Index. I used R script (v4.3.2, R Core Team, 2016) to plot a 75m radius circle
around each nest box in Google Earth (Google inc., 2021). I imported these images into GNU
image manipulation software (GIMP) (The GIMP team, 2023) and manually classified natural
(native grasses, trees, dirt, and bushes) and non-natural (lawn grass, pavement, and buildings)
habitat features for each image. I then grouped natural habitat features (native grasses, trees, bare
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earth, and bushes etc) and urban features (mowed lawns, pavement, and buildings etc) into a
single continuous index using a Principal Component Analysis (PCA) in RStudio (build 494,
2023-10-16).
The first principal axis (PC1) explained 67% of the variation and was the only axis to
explain more variation than explained by chance alone; therefore, it was the sole axis used in
classification. Proportion of the habitat including lawns pavement and buildings all had negative
values (all <-0.11) for PC1 and natural habitat had strongly positively values (0.54). As a result, a
negative PC1 value is associated with urban habitat and positive PC1 value with rural habitat,
and there was no overlap in the distributions, confirming the dichotomous nature of our habitat
groupings.
If the Urbanization index value for a certain nest was less than zero it was designated as
Urban and if the value was 0.5 or greater it was designated as rural. I chose 0.5 as the cut off for
urban nests since this index value corresponded to nest sites that had 25% or greater of the areas
surrounding the nestbox comprised of anthropogenic features. I used zero as the cut off for a nest
site being designated as urban to ensure that all nest designated as urban were strictly urban and
omitted three nests from all analyses.

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Figure 1.2 Google Earth image of typical mountain chickadee (Poecile gambeli) nest sites within the
study site in Kamloops, BC, Canada. The left image shows a typical rural site and the right shows a
typical urban site. The blue circle has a radius of 75m and demonstrates the approximate size of a
mountain chickadee’s territory. Photo credit; Google Earth pro

1.8 Thesis Overview
The goal of this thesis is to investigate how urbanization affects the nest ectoparasites of
mountain chickadees, and how this in turn affects both nestling development and parental
feeding behaviour. In Chapter 2, I enumerate the blowflies and fleas found in collected nests in
2019 and 2020, to determine whether nest parasitism differs between habitats and influences nest
success. In Chapter 3, I use video footage of feeding behavior to compare feeding rates between
habitats to determine whether there is evidence of compensatory feeding and see if this affects
growth rate of nestlings. Finally in Chapter 4, I synthesize my findings to consider how
differences between urban and rural environments in parasitism levels could affect nesting in
mountain chickadees, what this might tell us about adaptability to urban settlement, and possible
future research that could expand on my findings.

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1.9 References
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Applications, 6(2), 506–519. https://doi.org/10.2307/2269387
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(2017). Effects of parental condition and nesting habitat on sex allocation in the mountain
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Christe, P., Richner, H., & Oppliger, A. (1996). Begging, food provisioning, and nestling
competition in great tit broods infested with ectoparasites. Behavioral Ecology, 7(2), 127–
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Dijkstra, L., Florczyk, A. J., Freire, S., Kemper, T., Melchiorri, M., Pesaresi, M., & Schiavina,
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reveals a different picture of global urbanisation. Journal of Urban Economics, 125, 103312.
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induced by urbanization on bird local extinctions. Biological Conservation, 256, 109064.
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Eeva, T., & Klemola, T. (2013). Variation in prevalence and intensity of two avian ectoparasites
in a polluted area. Parasitology, 140(11), 1384–1393.
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Eeva, T., Lehikoinen, E., & Nurmi, J. (1994). Effects of ectoparasites on breeding success of
great tits (Parus major) and pied flycatchers (Ficedula hypoleuca) in an air pollution
gradient. Canadian Journal of Zoology, 72(4), 624–635. https://doi.org/10.1139/z94-085
Frainer, A., McKie, B. G., Amundsen, P.-A., Knudsen, R., & Lafferty, K. D. (2018). Parasitism
and the Biodiversity-Functioning Relationship. Trends in Ecology & Evolution, 33(4), 260–
268. https://doi.org/10.1016/j.tree.2018.01.011
García-Navas, V., & Sanz, J. J. (2012). Environmental and Within-Nest Factors Influencing
Nestling-Feeding Patterns of Mediterranean Blue Tits (Cyanistes caeruleus)—Factores
Ambientales y Sociales que Influyen en los Patrones de Aprovisionamiento de las Crías de
Cyanistes caeruleus. The Condor, 114(3), 612–621.
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Goater, T. M., Goater, C. P., & Esch, G. W. (2014). Parasitism: The Diversity and Ecology of
Animal Parasites. Cambridge University Press.
Gold, C. S., & Dahlsten, D. L. (1983). Effects of Parasitic Flies (Protocalliphora spp.) on
Nestlings of Mountain and Chestnut-Backed Chickadees. The Wilson Bulletin, 95(4), 560–
572.
Goodenough, A. E., Elliot, S. L., & Hart, A. G. (2011). Do orientation-based differences in
nestbox temperature cause differential ectoparasite load and explain patterns of nest-site
selection and offspring condition in great tits? International Journal of Zoology.
https://doi.org/10.1155/2011/514913
Grundel, R. (1987). Determinants of Nestling Feeding Rates and Parental Investment in the
Mountain Chickadee. The Condor, 89(2), 319–328. https://doi.org/10.2307/1368484

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Grundel, R. (1990). The Role of Dietary Diversity, Prey Capture Sequence and Individuality in
Prey Selection by Parent Mountain Chickadees (Parus gambeli). Journal of Animal Ecology,
59(3), 959–976. https://doi.org/10.2307/5025
Hajdasz, A. C., Otter, K. A., Baldwin, L. K., & Reudink, M. W. (2019). Caterpillar phenology
predicts differences in timing of mountain chickadee breeding in urban and rural habitats.
Urban Ecosystems, 22(6), 1113–1122. https://doi.org/10.1007/s11252-019-00884-4
Hanmer, H. J., Thomas, R. L., Beswick, G. J. F., Collins, B. P., & Fellowes, M. D. E. (2017).
Use of anthropogenic material affects bird nest arthropod community structure: Influence of
urbanisation, and consequences for ectoparasites and fledging success. Journal of
Ornithology, 158(4), 1045–1059. https://doi.org/10.1007/s10336-017-1462-7
Harriman, V. B., Dawson, R. D., Clark, R. G., Fairhurst, G. D., & Bortolotti, G. R. (2014).
Effects of ectoparasites on seasonal variation in quality of nestling Tree Swallows (
Tachycineta bicolor ). Canadian Journal of Zoology, 92(2), 87–96.
https://doi.org/10.1139/cjz-2013-0209
Hart, M. A., & Sailor, D. J. (2009). Quantifying the influence of land-use and surface
characteristics on spatial variability in the urban heat island. Theoretical and Applied
Climatology, 95(3), 397–406. https://doi.org/10.1007/s00704-008-0017-5
Heeb, P., Kölliker, M., & Richner, H. (2000). Bird–Ectoparasite Interactions, Nest Humidity,
and Ectoparasite Community Structure. Ecology, 81(4), 958–968.
https://doi.org/10.1890/0012-9658(2000)081[0958:BEINHA]2.0.CO;2
Hurtrez-Bousses, S., Blondel, J., Perret, P., Fabreguettes, J., & Renaud, F. R. (1998). Chick
parasitism by blowflies affects feeding rates in a Mediterranean population of blue tits.
Ecology Letters, 1(1), 17–20. https://doi.org/10.1046/j.1461-0248.1998.00017.x
Isaksson, C., & Andersson, S. (2007). Carotenoid Diet and Nestling Provisioning in Urban and
Rural Great Tits Parus major. Journal of Avian Biology, 38(5), 564–572.

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Koo Lee, J., Chung, O.-S., & Lee, W.-S. (2011). Altitudinal Variation in Parental Provisioning
of Nestling Varied Tits ( Poecile varius ). The Wilson Journal of Ornithology, 123(2), 283–
288. https://doi.org/10.1676/10-106.1
Kozlovsky, D. Y., Weissgerber, E. A., & Pravosudov, V. V. (2017). What makes specialized
food-caching mountain chickadees successful city slickers? Proceedings of the Royal
Society B: Biological Sciences, 284(1855), 20162613.
https://doi.org/10.1098/rspb.2016.2613
Kurucz, K., Purger, J. J., & Batáry, P. (2021). Urbanization shapes bird communities and nest
survival, but not their food quantity. Global Ecology and Conservation, 26, e01475.
https://doi.org/10.1016/j.gecco.2021.e01475
LaZerte, S. E., Otter, K. A., & Slabbekoorn, H. (2017). Mountain chickadees adjust songs, calls
and chorus composition with increasing ambient and experimental anthropogenic noise.
Urban Ecosystems, 20(5), 989–1000. https://doi.org/10.1007/s11252-017-0652-7
Loye, J., & Carroll, S. (1995). Birds, bugs and blood: Avian parasitism and conservation. Trends
in Ecology & Evolution, 10(6), 232–235. https://doi.org/10.1016/S0169-5347(00)89072-2
Marini, K. L. D., Otter, K. A., LaZerte, S. E., & Reudink, M. W. (2017). Urban environments are
associated with earlier clutches and faster nestling feather growth compared to natural
habitats. Urban Ecosystems, 20(6), 1291–1300. https://doi.org/10.1007/s11252-017-0681-2
McCallum, D. A., Grundel, R., & Dahlsten, D. L. (2020). Mountain Chickadee (Poecile
gambeli), version 1.0. Birds of the World. https://doi.org/10.2173/bow.mouchi.01
Mock, D. W. (2022). Parental care in birds. Current Biology, 32(20), R1132–R1136.
https://doi.org/10.1016/j.cub.2022.07.039
Musgrave, K., Bartlow, A. W., & Fair, J. M. (2019). Long‐term variation in environmental
conditions influences host–parasite fitness. Ecology and Evolution, 9(13), 7688–7703.
https://doi.org/10.1002/ece3.5321

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O’Brien, E. L., & Dawson, R. D. (2008). Parasite-Mediated Growth Patterns and Nutritional
Constraints in a Cavity-Nesting Bird. Journal of Animal Ecology, 77(1), 127–134.
Pickett, S. T. A., Cadenasso, M. L., Grove, J. M., Boone, C. G., Groffman, P. M., Irwin, E.,
Kaushal, S. S., Marshall, V., McGrath, B. P., Nilon, C. H., Pouyat, R. V., Szlavecz, K.,
Troy, A., & Warren, P. (2011). Urban ecological systems: Scientific foundations and a
decade of progress. Journal of Environmental Management, 92(3), 331–362.
https://doi.org/10.1016/j.jenvman.2010.08.022
Preston, D., & Johnson, P. (2010). Ecological Consequences of Parasitism. Nature Education
Knowledge, 3(10), 47.
R Core team. (2023). R: A Language and Environment for Statistical Computing (4.3.1)
[Computer software]. R Foundation for Statistical Computing.
Rocha, C. F. D., Bergallo, H. G., & Bittencourt, E. B. (2016). More than just invisible
inhabitants: Parasites are important but neglected components of the biodiversity. Zoologia
(Curitiba), 33, e20150198. https://doi.org/10.1590/S1984-4689zool-20150198
Ruas, R. de B., Costa, L. M. S., & Bered, F. (2022). Urbanization driving changes in plant
species and communities – A global view. Global Ecology and Conservation, 38, e02243.
https://doi.org/10.1016/j.gecco.2022.e02243
Schwagmeyer, P. L., & Mock, D. W. (2008). Parental provisioning and offspring fitness: Size
matters. Animal Behaviour, 75(1), 291–298. https://doi.org/10.1016/j.anbehav.2007.05.023
Seress, G., & Liker, A. (2015). Habitat urbanization and its effects on birds. Acta Zoologica
Academie Scientarium Hungaricae, 61(4), Article 4.
Sinkovics, C., Seress, G., Pipoly, I., Vincze, E., & Liker, A. (2021). Great tits feed their nestlings
with more but smaller prey items and fewer caterpillars in cities than in forests. Scientific
Reports, 11(1), Article 1. https://doi.org/10.1038/s41598-021-03504-4

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Smith, B. L., Snell, C. L., Reudink, M. W., & Otter, K. A. (2022). Urban-nesting mountain
chickadees have a reduced response to a simulated predator. Behaviour, 159(3/4), 301–320.
https://doi.org/10.1163/1568539X-bja10122
Tripet, F., Glaser, M., & Richner, H. (2002). Behavioural responses to ectoparasites: Timebudget adjustments and what matters to Blue Tits Parus caeruleus infested by fleas:
Behavioural responses of Blue Tits to ectoparasites. Ibis, 144(3), 461–469.
https://doi.org/10.1046/j.1474-919X.2002.00018.x
Tripet, F., & Richner, H. (1997). Host Responses to Ectoparasites: Food Compensation by Parent
Blue Tits. Oikos, 78(3), 557–561. https://doi.org/10.2307/3545617
Tripet, F., & Richner, H. (1999). Dynamics of Hen Flea Ceratophyllus gallinae Subpopulations
in Blue Tit Nests. Journal of Insect Behavior, 12(2), 159–174.
https://doi.org/10.1023/A:1020958615191
UN-Habitat. (2023). Rescuing SDG 11 for a Resilient Urban Planet. SDG 11 SYNTHESIS
REPORT HIGH LEVEL POLITICAL FORUM 2023.
US EPA, O. (2015, November 3). Urbanization—Overview [Collections and Lists].
https://www.epa.gov/caddis-vol2/urbanization-overview
Wesołowski, T. (2001). Host–parasite interactions in natural holes: Marsh tits ( Parus palustris )
and blow flies ( Protocalliphora falcozi ). Journal of Zoology, 255(4), 495–503.
https://doi.org/10.1017/S0952836901001571
Williams, T. D. (2018). Physiology, activity and costs of parental care in birds. Journal of
Experimental Biology, 221(17), jeb169433. https://doi.org/10.1242/jeb.169433

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CHAPTER 2: BLOWFLY AND FLEA INFESTATION OF MOUNTAIN CHICKADEE
NESTS

2.1 Introduction
Urbanization has many interacting impacts on the environment, including meteorological
changes (particularly temperature), light pollution, noise pollution, and changes in vegetation
(Serres and Liker, 2015). The effects of urbanization have significant impacts on biological
communities and their structure. How birds respond to urbanization and whether they can
exploit, acclimate to, or must avoid urban environments, depends on how urbanization affects
their food sources and predators, including parasites as well as the ecology and life history traits
of each species (Blair, 1996).
Blood-feeding ectoparasites can impact the size, mortality and body condition of nestlings as
well as the reproductive success and health of adult birds (Goater et al., 2014; Loye and Carroll,
1995; Musgrave et al., 2019). However, other studies have found ectoparasites to have little to no
effect on nesting birds (Musgrave et al., 2019). The degree of harm caused by parasites on their
hosts is variable, influenced by both the variety of parasite species present in nests, and
interactions between parasites and nest microenvironment. Thus, environmental changes due to
urbanization that influence parasites may directly impact bird communities (Goater et. al., 2014).
The most common nest ectoparasites of cavity nesting birds in North America are fleas
(Siphonaptera) and blow flies (Diptera: Calliphoridae) (Heeb et al., 2000). The most common
bird fleas are in the genus Ceratophyllus (Tripet and Richner, 1999), which live in the nest
material and emerge to take blood meals from nestlings and brooding adults (Tripet and Richner,
1999). Two generations of fleas live in the nest at the same time. The colonizing adult fleas (F0)

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feed on the parent birds during the egg laying and incubation phase and then lay eggs in the nest
material that hatch into first generation larvae (F1). These larvae feed on detritus present in the
nest material and then form cocoons that hatch during the nesting period. The first-generation
adults feed on the nestlings and lay eggs that hatch into second generation larvae (F2) that form
cocoons toward the end of the nestling period. Second generation adults emerge in the winter
months after the young fledge and either disperse or overwinter in the nest (Tripet and Richner,
1999).
The blow flies that typically affect bird nestlings are in the genus Protocalliphora (Sabrosky
et al., 1989). Adult flies overwinter outside of the nest in sheltered places like hollow trees and
then mate in early spring (Bennett and Whitworth, 1990). Females lay eggs in nest cavities once
nestlings hatch, and larvae feed on the nestlings until the maggots reach their final instar and
pupate (Wesolowski, 2001). Similar to adult fleas, bird blow fly larvae spend most of their time
in the nest material and only emerge to obtain blood meals from nestlings (Roby et. al., 1992).
Blood feeding by parasites can kill nestlings outright, but more often it results in anemia,
reduced growth rates, and poor body condition (Reviewed in Loye and Carroll, 1995). Removal
or reduction of parasites in the nest can result in improved nestling condition and survival.
Hurtrez-Boussès et al. (1998) observed that blue tit (Cyanistes caeruleus) nestlings in nests that
had Protocalliphora larvae removed exhibited higher growth rates, higher body mass at fledging,
higher hematocrit levels, and longer tarsi than nestlings in parasitised nests. Similarly, Harriman
et al. (2014) found that tree swallow (Tachycineta bicolor) nestlings in nests where blow flies
and fleas had been removed had higher growth rates than control nests at one study site (Prince
George, BC), but not the other (St. Denis National Research Area, Saskatchewan). Adult birds
and nestlings may behaviourally compensate for the impact of parasites by increasing the rate of

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feather and nest grooming behaviours or compensatory feeding (Tripet and Richner, 1997;
Harriman et al., 2014). A major factor that controls the numbers of parasites present in nests (and
hence the potential impact on nesting birds) is the microclimate of the nest (temperature,
humidity etc.).
Nest microclimate not only influences survival of parasite larvae, but weather conditions
also influence the capacity of adult parasites to find and lay eggs in the nest. Insects have an
optimal temperature for development and survival; cold temperatures can slow development and
hot temperatures can cause deformities or mortality in developing larvae (Dawson et al, 2005).
Dawson et al. (2005) found that the abundance of Protocalliphora in experimentally heated tree
swallow nests increased gradually up to 25°C, but declined as temperatures in the nest increased
above this threshold. Because the location of a nest has a strong influence on the temperature
within the nest box, nests in urban areas may experience warmer conditions due to the Urban
Heat Island effect compared to rural nests, thus impacting parasite survival and reproduction
(Sonnenberg et al., 2020).
First documented in 1833, the Urban Heat Island effect is a well recognized meteorological
phenomenon where urban areas can be as much as 10 degrees warmer than corresponding rural
areas (Pickett et al., 2011). Urban areas have significant changes in vegetation and plant
communities relative to rural areas (Ruas et al., 2022). Land use change results in a reduction in
the density and distribution of plants, the amount of non-native plant species and the level of
species richness (Ruas et al., 2022). Loss of vegetation and an increase in dark surfaces (due to
the use of asphalt and concrete in roads and buildings) result in higher air temperatures due to the
reduction in surface albedo and evapotranspiration (Akbari et al., 2001). Nests in urban
environments could experience earlier springs and more consistent, warm temperatures

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throughout the nesting cycle that promote increased rates of parasitism, and increased density
and development of parasitic larvae.
The parasite release hypothesis is the idea that species that do well in urban environments
may do so because their parasites are less common there (Le Gros et al. 2011). There have been
multiple studies that indicate that urbanization can reduce the abundance of some types of
parasites. Le Gros et. (2011) found that Philornis porteri (Diptera: Muscidae) were less prevalent
in northern mockingbird (Mimus polyglottos) nests in parking lots and residential neighborhoods
and more prevalent in nests in nature preserves and pastures (Le Gros et. al., 2011). Hanmer et.
al. (2017) found no correlation between habitat urbanization and flea abundance in blue tits
(Cyanistes caeruleus) but did find that increasing urbanization led to lower flea abundance in
great tit nests (Parus major) due to increased inclusion of anthropogenic material.
If urbanization reduces the numbers of ectoparasites in nests it would result in a reduction of
the parasitic impact on urban birds relative to rural birds. This reduction in parasitic impact may
compensate for the pressures of urbanization or even result in improved survival and growth of
nestling birds and adults in urban nests relative to birds in rural nests. The removal or reduction
of parasites may be one of the aspects of urbanization that influences whether birds are able to
adapt to or exploit urban environments.
The mountain chickadee (Poecile gambeli) is a small cavity nesting songbird that inhabits
the mountainous conifer forests of western North America (Campbell et al., 2007). Research
comparing the urban and rural populations of mountain chickadees in Kamloops British
Columbia, Canada showed no negative impacts of urbanization on clutch size, nest success, or
nestling growth, suggesting they can cope with urbanization (Marini et. al., 2017). My interest

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lay in determining whether lower ectoparasite loads in urban nests may be contributing to
nesting behaviour of urban chickadees.
Over two field season I collected data on mountain chickadees in Kamloops, BC, to examine
how ectoparasite loads impact mountain chickadees breeding in urban and rural habitats and how
ectoparasite loads and environmental changes associated with urbanization are related. In line
with the parasite release hypothesis, I predict that urban nests will have fewer parasites and
fledge more young. Based on the Urban Heat Island effect and other ecological changes typically
associated with urbanization I predicted that urban nests would be warmer and have less
vegetation surrounding them.

2.2 Methods
2.2.1 Nest location and monitoring
I describe the study site in detail in Chapter 1, section 1.5, general field methods in Chapter 1,
section 1.6, and how urbanization status was designated in Chapter 1, section 1.7. I monitored 23
mountain chickadee nests in 2019 (11 from urban nests and 12 from rural nests) and 21 nests in
2020 (10 urban and 11 rural)
Once nest building activity, such as the removal of woodchips or the appearance of a grass
nest cup within an individual nest box was observed, we added an Onset HOBO Pendant
Wireless Temperature and Light Data Logger (model MX2202) to top of the nest box. These
collected temperature and light data continuously at intervals of 1 second and allowed us to
determine hourly temperatures at each nest during critical parts of the nesting cycle. I
downloaded the data from the loggers once a month using the HOBOmobile app on my phone.
Data output from the loggers was presented in a temperature per second format. For analysis, I
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converted the data to maximum, minimum, and mean daily temperature. I then calculated the
average temperature at each nest for the period between the start of incubation and the hatching
date (which I will hereafter refer to as the incubation period), and between the hatching and
fledging dates (which I will hereafter refer to as the nestling period).
2.2.2 Nest collection
I collected 23 mountain chickadee nests in 2019 (11 from urban nests and 12 from rural nests)
and 21 nests in 2020 (10 urban and 11 rural) one to three days after fledging. The nests were
collected once all nestlings and parents had left the nest box area and displayed no evidence of
renesting behaviour, such as the addition of new nesting material or freshly laid eggs. Due to
weather conditions during collection in 2020, five nests (4 rural and 1 urban) became wet, which
kills flea larvae. This can differentially affect estimation of flea abundance, but not the blow fly
abundance as blow flies are already developed enough to count prior to incubation (Heeb et. al.,
2000). Blow fly larvae form puparia while nestlings are still in the nest, so even if they are killed
they can still be counted. As a result, I excluded these nests from analyses on flea abundance, but
was able to include them on analyses of blow fly abundance.
I removed nests and all sub-nest substrate (wood shavings) from the nest boxes with gloved
hands, and placed them in a labelled, sealed freezer bag. The collected nest material was left in a
dark container to incubate within the freezer bags for a minimum of 15 days and a maximum of
20 days until adult fleas and blow flies were visible in the bags. I then placed the bags containing
the nest material in a -20°C freezer for at least one month to ensure all living arthropods in the
nests were dead.

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After a 2-hr thawing period I removed the nests from the bag and placed them in a tray for
sorting; larger volume nests were subdivided for ease of sorting. I used tweezers to remove adult
blow flies, blow fly puparia, fleas, and other objects of note (such as parasitoid wasps) through
visual inspection. After I removed nest debris and fur from the specimens, I placed fleas and
blow flies in labeled vials containing at least 80% ethyl alcohol.
2.2.3 Parasite identification
Due to large sample sizes (as many as 387 fleas), samples of fleas containing more than 20
specimens were subsampled to include 10 males and 10 females. I placed the selected adult fleas
in a 10% potassium hydroxide solution to dissolve all soft tissues for 24 hours (clearing). After
the clearing procedure I placed the fleas into a dilute acetic acid (1%) solution for 30 minutes
and then into distilled water for another 30 minutes. I then dehydrated the fleas by putting them
through series of alcohol solutions (70%, 90% and 100%) for a minimum of 30 minutes at each
concentration. To make the chitin more transparent and make the internal and external structures
more visible, I transferred the dehydrated fleas to methyl salicylate for ten minutes before
transferring the fleas to xylene for a minimum of one hour to prepare for mounting. I mounted
the fleas in Canadian balsam diluted with xylene to bring the Canadian balsam to a more
workable viscosity. These mounting procedures were adapted from Nelson (2001). Once the
fleas were mounted on slides, they were placed in a 40°C drying oven for at least a month. Fully
cured slides were allowed to cool and then identified to species based on Lewis and Galloway
(2001).
I identified blow flies to genus based on Whitworth (2003) due to the difficulty in
identifying blow flies to species based on potentially broken puparia. Due to the challenging

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nature of identifying fly species through morphology, DNA barcoding is often used to identify
flies to species (Meiklejohn et al, 2013), a method that was outside the scope of this project.
Based on finding only one genus of blow fly and one species of flea in the 2019 samples, I
simply counted the number of fleas and blow flies collected from the nests in 2020, all analyses
are based on these grouped samples. Counts are based on numbers of adult fleas and numbers of
blow fly puparia. Puparia were counted as opposed to adult flies because puparia counts provide
a more accurate estimate of the number of feeding larvae in the nest and are not subject to
attrition through failure to pupate due to parasitoid infestation or other mortality factors.
2.2.4 Statistical analysis
Blow flies
I investigated several factors hypothesized to affect blow fly abundance in the examined nests;
these include the habitat type (urban/rural), Julian date of initiation of incubation, and mean
ambient temperature during the nestling period of the nesting cycle. I used a generalized linear
mixed-effects model (R package glmmTMB, Brooks et. al., 2023) to compare the total number
of blow flies (puparia) collected from each nest against several fixed effects: Urban/Rural
classification; Year of sampling (2019 and 2020); Julian date of initiating incubation; and mean
temperature during the nestling period. I specified a zero-inflated Poisson distribution of blow
fly counts. I initially included each pairwise interaction added to the model, and sequentially
removed non-significant interactions (P>0.1) until only the main effects (individual variables)
and significant interactions remained. The final model included habitat status, maximum
temperature during the nestling period, and year as fixed effects.

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Fleas
I similarly developed a generalized linear mixed-effects model to test similar habitat and
temperature variable as influencing flea abundance (R package glmmTMB, Brooks et. al., 2023).
In this analysis, however, the temperature during the incubation period was used, as temperature
is most important for flea development during this period (Tripet and Richner, 1999). As
described above, I initially included all main effects and interaction terms in the models and
tested the remaining main effects with all pair-wise interaction terms. I sequentially removed the
non-significant interaction terms (P>0.1) until I was left with the main effects (mean temperature
during the incubation period, habitat status, and year).
Nest success
I generated a generalized linear mixed-effects model to assess the potential effect of the number
of blow flies, fleas, and year on nest success (represented as the number of fledged offspring)
with the number of eggs as random effects to control for the initial number of offspring. I
generated a second generalized linear mixed-effects model to assess the effect of habitat and
mean ambient temperature during the incubation period on nest success with the number of eggs
as random effects to control for the initial number of offspring like the previous model. Mean
temperature during the incubation period was selected as incubation temperature is an important
factor in hatching success and nestling growth and therefore nest success (Nord and Nilsson,
2011, de Zwaan et. al., 2020).

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2.3 Results
2.3.1 Identifications
All of the blow fly puparia I examined were in the Genus Protocalliphora. The diagnostic
features used to distinguish this genus from others was the presence of a prothoracic fringe and
three distinct ventral spine bands (Bennett and Whitworth, 1991). All of the fleas I examined
were Ceratophyllus niger. I based this designation mostly on male specimens. The diagnostic
features I used to distinguish this species from the similar C. gallinae were the long, dorsally
spiculate, and blade-like vexillum at the end of sternite VIII, the three sectioned apex of sternite
IX, and the size of the movable process relative to the fixed process of the clasper (Lewis and
Galloway, 2001). I identified the females to C. niger based on the shape of sternite VII and the
level of sclerotization of the bursa copulatrix and the ductus obsturatus (Lewis and Galloway,
2001).

2.3.2 Abundance of blow fly puparia relative to urbanization, ambient temperature, and
year.
I found that habitat (estimate= -0.85+ 0.38SE, z = -2.26 p=0.024) and year (estimate= -1.58+
0.60SE, z =-2.61, p= 0.0088) had a significant association with the number of puparia, but the
maximum temperature during the nestling period did not (estimate=0.034 + 0.042SE, z = 0.83,
p= 0.41). Overall 2019 had higher maximum temperature than 2020, but urban areas tended to be
warmer than rural areas (Fig 2.1). Urban sites had fewer puparia (25.50+9.86SE) than rural sites
(38.65+8.78SE) (Fig 2.2).

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Figure 2.1 Boxplot comparing the maximum temperature during the nestling period during 2019 and 2020
comparing urban and rural environments
.

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.

Figure 2.2 Boxplot the number of puparia found in nests during 2019 and 2020 comparing urban and rural
environments.

2.3.3 Abundance of adult fleas relative to urbanization and year.
I found that mean temperature during the incubation period (estimate=0.47 +0.19SE, z =2.44,
p=0.015) and year (estimate=1.50+0.69SE, z =2.20, p=0.031) had a significant association with
the number of fleas but habitat status did not (estimate= -0.38+0.48SE, z =-0.79, p=0.43).
Overall 2019 had higher maximum temperature than 2020, but urban areas tended to be warmer
than rural areas (Fig 2.3). The mean number of fleas per nest was greater in
2020(78.92+34.01SE) than in 2019 (48.14+16.17SE). Urban sites (61.46+23.60SE) tended to
have more fleas present than rural sites(59.86+22.86SE), though this was not statistically
significant (Fig 2.4).
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Figure 2.3 Boxplot comparing the mean temperature during the incubation period during 2019 and 2020
comparing urban and rural environments.

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Figure 2.4 Boxplot comparing the number of fleas found in nests during 2019 and 2020 comparing urban
and rural environments.

2.3.4 The effect of parasites and habitat type on number of chicks fledged.
The number of chicks fledged was not associated with the number of blow flies in the nest
(estimate=-0.00010+0.001, z=-0.086, p=0.93), the number of fleas (estimate=0.0001+0.0004SE,
z=-0.35, p=0.73), year (estimate=0.033+0.094SE, z=0.36, p=0.72) or mean ambient temperature
during the incubation period (estimate=-0.048+0.028SE, z=-1.70, p= 0.089) but it was associated
with habitat type (estimate=0.22+0.41SE, z=2.15, p= 0.032). Urban nests had significant more
chicks fledged (6.14+0.40SE) than rural nests (5.15+0.34SE), with urban nests fledging
approximately one additional chick per nest (Fig 2.5).

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Figure 2.5 Boxplot comparing the number of chicks fledged in urban and rural environments.

2.4 Discussion
My results showed that rural sites had greater number of puparia in both years and 2019 had
more puparia relative to 2020. The number of fleas wasn’t associated with habitat, but there was
both a temperature and year affect. Within each year of the study, urban nests were warmer on
average than rural nests during both the incubation and nestling period. The number of chicks
fledged was not affected by either nest ectoparasite or year but was associated with habitat type
with urban nests fledging approximately one additional chick per nest (Fig 2.5).
Weather can have consequences on ectoparasitese that only live on hosts for a portion of
their life cycle, with temperature extremes impacting both development of larval stages as well
as the ability of adults to successfully mate and deposit eggs (Merino and Potti, 1996). All

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poikilotherms have an optimal temperature at which developmental rate peaks. Development
may be halted if temperature is too low, while too high temperature may result in deformity or
death (Dawson et. al., 2005).
2.4.1 Blow flies
Temperature has a significant effect on the ectoparasitic larval stage of Protocalliphora and
other related blow flies (Bennett and Whitworth, 1991). Although they experience mild
temperature shifts since they are not constantly feeding and move between the host and the nest
material, significant deviation from the typical temperatures in the nest cavity significantly
affects Protocalliphora larvae survival and growth (Dawson et. al., 2005). In multiple studies a
significant and positive relationship between temperature and puparia abundance has been
observed (Castaño-Vázquez and Merino, 2022; Dawson et al., 2005). Dawson et al. (2005) found
that Protocalliphora in tree swallow (Tachycineta bicolor) nests increased in abundance with
increasing temperature between 15°C and 25°C. Both urban (26.9+1.53°C) and rural
(24.6+1.48°C ) sites had average maximum temperatures close to the 25°C optimum determined
by Dawson et al. (2005). While urban sites were warmer than rural sites, which has led to
increased number of puparia in other studies, urban sites in our study had fewer puparia than
rural sites and there was no significant relationship between temperature and numbers of puparia.
This suggests that a factor other than temperature is responsible for the differences between
urban and rural pupa abundance.
As oviposition by free living adults is necessary for puparia to be present in nests, the
abundance of adult Protocalliphora likely affects the abundance of pupa in nests. One of the
factors used to determine urbanization status in this study was the presence or lack of native
vegetation around each nest site; urban sites were classified as having less native vegetation
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around them. While blow flies are typically associated with carrion feeding, experiments have
demonstrated that Protocalliphora are not carrion feeders, with a possible exception of gravid
females (Bennett and Whitworth, 1991). Adult blow flies did not feed on meat when presented
with it and the natural food source they fed on was pollen from wildflowers and fruit (Bennett
and Whitworth, 1991). Field observations also indicate that adult blow flies mostly feed on
flowers (Bennett and Whitworth, 1991).
Protocalliphora prevalence is associated with areas that have greater amounts of vegetation
(Eeva and Klemola, 2013). Other studies have attributed lower prevalence of blow flies in
disturbed areas to degradation of natural vegetation and the use of pesticides (Moreno-Rueda,
2021). The lower abundance of blow fly puparia in urban areas observed in this study may be
due to reduced amount of native vegetation, which contributes to lower abundance of adult blow
flies available to oviposit in nests due to reduced food and shelter.
2.4.2 Fleas
As with many insects, flea survival is closely tied to temperature. Increasing temperature can
have a positive effect on flea abundance and the heat provided by the incubating female within
the nest is important for the emergence of adult fleas from cocoons (Castano-Vasquez and
Merino 2022; Tripet and Richner, 1999). Bird fleas either overwinter in the nestbox or are
brought into the nest on adult birds; the lack of a free-living stage outside nests makes conditions
within the nest more important to flea abundance than pupa abundance (Tripet and Richner,
1998; Rendell and Verbeek, 1996). Despite the importance of temperature in flea survival and
development, the relationship between temperature and flea abundance varies significantly in
studies that explore this relationship. Some studies have found a positive relationship between
fleas and temperature whereas others have found a negative relationship between fleas and
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temperature or even no relationship at all (Castano -Vasquez and Merino, 2022; CastanoVasquez et al., 2021; Goodenough et. al., 2011, Krasnov et al., 2001). In this study I found that
significantly more fleas were found in nests in 2020, the cooler of the two sampling years. This,
along with the significant relationship between flea abundance and temperature, suggests that
cooler temperatures may favour the survival and development of fleas at my study site. The
experimental heating of nest boxes by as little as 2°C can reduce the abundance of flea larvae in
nests, although this effect may be tied to the climatic conditions of the study area (CastanoVasquez et al., 2018; Castano-Vasquez et al., 2021; Garcia del Rio, 2023). In Castano-Vasquez
et al. ( 2021) a significant change in larval flea abundance was only observed in the warmer and
drier study site, which they attributed to the difference in the change in humidity observed
between the two sites. The differing ways that temperature affects other micro climatic aspects of
a given study site may be responsible for the range of results observed in studies of fleas and
temperature. Humidity, an important aspect of microclimate itself, may moderate how
temperature increases in the nest box affect fleas, leading to greater impact of increasing
temperatures in less humid environments (Heeb et al., 2000; Castano-Vasquez et al., 2021;
Garcia del Rio, 2023). Kamloops has a semi-arid climate which may have contributed to a
negative impact of increasing temperature on flea abundance which would explain the lower
abundance of fleas in the warmer year of sampling.
2.4.3 Nest success
While both fleas and blow fly larvae can have impacts on nestling growth and survival there
was no relationship between the abundance of either fleas or blow flies on the number of chicks
fledged in each nest, although urban nests fledged approximately one more chick than urban
nests. Finding no noticeable effect of parasitism on survival or growth rate of nestlings is not

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uncommon in studies of ectoparasites of birds. Studies on tree swallows failed to find a
relationship between nestling quality (body size and plumage quality) and ectoparasite load
(Thomas and Shutler, 2001; Harriman et al., 2013). Similarly, Goodenough et. al. (2011)
observed no correlation between flea abundance and blue tit nestling quality and proposed that
the true impact of parasitism may be increased parental cost and masked fitness costs in the
nestlings. Parental cost is an adaptive increase in parental provisioning rates and nest sanitation
by parent birds (Goodenough et. al., 2011). This behaviour can transfer the costs and impacts of
parasitism from the offspring to the parent through the increased metabolic costs of this
behaviour. The impact of parasitism on young birds can be masked by other factors affecting
fitness like hatching order and the territory quality. Parents may compensate for the impact of
blow fly larvae by increasing their feeding rate by as much as 65% in infested nests relative to
non-infested nests (Hurtrez-Bousses et al., 1998). Reduction in blow fly abundance would reduce
feeding pressure on parents and allow chicks to spend less time on anti-parasitic behaviours such
as grooming, thereby reducing metabolic costs for both chicks and parents (Hurtrez-Bousses et
al., 1998; Simon et al., 2005)
The environmental changes associated with urbanization may be creating a refuge from
parasites for mountain chickadees in urban Kamloops (Gsell et. al. 2013). The partial removal of
parasitic pressure may lead to a reduced need for compensatory feeding or other behavioral ways
of mitigating the cost of parasitism. The absence of negative impacts of urbanization on clutch
size, nest success, or nestling growth in Kamloops may be due to reduced parasitic pressure on
the nestlings in urban areas and the resulting reduction in pressure on parents for increased
feeding. Additionally reduced parasitism on parents and reduced need for compensatory feeding
of nestlings by parents may result in improved parental condition in urban areas.

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Sonnenberg, B. R., Branch, C. L., Benedict, L. M., Pitera, A. M., & Pravosudov, V. V. (2020).
Nest construction, ambient temperature and reproductive success in a cavity-nesting bird.
Animal Behaviour, 165, 43–58. https://doi.org/10.1016/j.anbehav.2020.04.011
Thomas, K., & Shutler, D. (2001). Ectoparasites, nestling growth, parental feeding rates, and
begging intensity of tree swallows. Canadian Journal of Zoology, 79(2), 346–353.
https://doi.org/10.1139/z00-206
Tripet, F., & Richner, H. (1999). Dynamics of Hen Flea Ceratophyllus gallinae Subpopulations
in Blue Tit Nests. Journal of Insect Behavior, 12(2), 159–174.
https://doi.org/10.1023/A:1020958615191
Whitworth, T. L. (2003). A key to the puparia of 27 species of North American Protocalliphora
Hough (Diptera: Calliphoridae) from bird nests and two new puparial descriptions.
Proceedings of the Entomological Society of Washington, 105, 995-1033.

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CHAPTER 3: PROVISIONING RATES OF MOUNTAIN CHICKADEES IN URBAN
AND RURAL HABITAT
3.1 Introduction
For altricial species, the rate at which parents provision their nestlings can directly impact
nestling growth rate; meanwhile, limited food availability and energetic costs of provisioning can
negatively affect parental condition and future reproductive success (VanBalen, 1973; HurtrezBoussès et al.,1998; Richner and Tripet 1999). Feeding rate depends on food availability, the
quality of available food, and the number of nestlings. (Grundel, 1987;; Sinkovics et al., 2021).
Another factor that increases feeding rate are factors that cause nestlings to require a greater
caloric input such as blood feeding by ectoparasites and weather (Tripet and Richner, 1997;
Harriman et al., 2014). For species that breed in urban areas, all these factors—from diet to
climate to parasite pressure—may be directly impacted by urbanization, leading to changes in
provisioning rates and, ultimately, reproductive success.
When either food quality or nestling condition is reduced, parents may have to increase their
feeding rate to maintain growth and development. For example, climate conditions, such as low
temperatures or unfavourable weather, can increase metabolic demands on nestlings; this can
increase nestling begging rate and result in a higher feeding rate by parents to meet demands
(Koo Lee et al.,2011). Parents may also reduce feeding rate in response to extreme conditions,
such as high temperatures that make foraging hazardous (García-Navas and Sanz, 2012).
Urbanization can significantly modify the environment birds live in and, in turn, may affect
feeding rates. Urban areas may be significantly warmer than rural areas and, as noted above,
temperature can impact feeding rates in birds (Meinke et al., 2013; Seress and Liker, 2015).

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Land-use changes associated with urbanization reduce overall plant cover and this in turn can
reduce the amount of insect prey available (Seress and Liker, 2015; Ruas, 2022). Further, the
vegetational composition in urban areas is often comprised of non-native plants, which may
modify the availability of native prey (Seress and Liker, 2015; Ruas, 2022). With a reduction in
available insect prey, urban birds are forced to feed nestlings lower quality food and/or increase
provisioning rates. Sinkovics et al. (2021) found that great tits (Parus major) in urban areas had a
greater feeding rate than in rural areas, but only in two out of the three years examined. This
increase in feeding rate was associated with reduced average prey volume; in short, both urban
and rural birds fed their nestlings similar amounts of food, but urban birds fed lower quality food
more often. Not all urban environments, however, are associated with changes in either the
abundance or quality of insect prey. Kurucz et al. (2021) observed no relationship between the
abundance of arthropods and the degree of urbanization, and even found a greater abundance of
insectivorous birds in urban areas suggesting they were able to cope with urbanization.
Often, we predict that species associated with specialized habitat requirements that are
lacking or reduced in urban landscapes will avoid these habitat types (Blair 1996); however, in
some cases such species not only occupy urban landscapes but are able to easily acclimate or
potentially adapt to these urban environments. Research comparing the urban and rural
populations of Mountain Chickadees in south-central British Columbia, Canada showed no
negative impacts of urban settlement on clutch size, nest success, or nestling growth, suggesting
they can cope with urbanization (Marini et. al., 2017). Although previous studies suggest overall
prey availability may be lower in urban vs rural habitats in this population (Hajdasz et al. 2019),
urban birds appear to adjust their nesting cycle to align with the local peak in prey availability
within their territories. This may allow the birds to offset some of the costs associated with urban

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settlement. Further, in Chapter 2, I show that urban nests in this population have reduced levels
of blood-feeding nest parasites (blow flies) compared to rural nests. As both time spent on
antiparasitic behaviours (such as grooming) and blood loss from ectoparasite infestation increase
the metabolic costs of nestlings, parents may have to compensate by increasing provisioning
rates (Hurtrez-Boussès et al.,1998; Knutie et al., 2016). This increase in feeding rate can be quite
significant; increases in feeding rate of as much as 70% have been observed in other studies
where parasite infestation is elevated (Hurtrez-Boussès et al.,1998; Knutie et al., 2016, Christe et
al. 1996). As such, the reduction in nestling parasites in urban mountain chickadee nests may
help offset reduced prey abundance in these habitats and help dampen the need for compensatory
parental feeding.
In this study, I further explore whether mountain chickadees adjust to urban settlement,
particularly in provisioning rates to nestlings. Using videos captured at individual nests, I
examine the effect of urbanization on feeding rates of mountain chickadee parents occupying
nests in Kamloops B.C.. If the reduction in nestling ectoparasites elevates the condition of urban
nestlings, I predict that parental feeding rates will be more elevated in rural habitats to
compensate. However, if the difference in relative insect prey abundance is higher in rural than
urban territories, as suggested by Hajdasz et al. (2019), urban parents will compensate for the
reduction in preferred prey and feeding rates would be higher in this habitat. If, though, the
complex interplay of reduced prey in one habitat is offset by reduced parasites in that habitat as
well, then feeding rates between habitats and nestling survival will not differ

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3.2 Methods
I describe the study site in detail in Chapter 1, section 1.5, general field methods in Chapter 1,
section 1.6, and how urbanization status was designated in Chapter 1, section 1.7.
Growth Rates were determined by change in wing chord length between day 6-9 following
Marini et al. (2017). Nests were then monitored for continued parental activity on day 15; any
nests that were still active at day 15 were considered to have reached successful fledging, as
mountain chickadees typically fledge around day 16, and disturbance to the nest tree after day
13-14 is likely to cause premature fledging (McCallum et. al., 2020, Gold and Dahlsten, 1983).
In 2019, temperature probes (Onset HOBO Pendant Wireless Temperature and Light Data
Logger (model MX2202)) were placed on the tops of nest boxes to collect micro-climate data
around the nests. These devices were installed as soon as a nest box was deemed to be active
and were attached to the roof of the box with tacks. I collected 23 mountain chickadee nests in
2019 (11 from urban nests and 12 from rural nests) and 21 nests in 2020 (10 urban and 11 rural)
one to three days after fledging. The nests were collected once all nestlings and parents had left
the nest box area and displayed no evidence of renesting behaviour, such as the addition of new
nesting material or freshly laid eggs. I incubated the collected nests 20 days at room temperature
(see Chapter 2) to enumerate the presence of blowfly parasites (Protocoliphera sp.) in individual
nests.
3.2.1 Video recording
In 2019, I recorded the frequency of feeding visits using GoPro HERO7 cameras pointed
towards the nest box entrance (see figure 3.1). I attached the nest cameras to a branch or other
structure adjacent to, and approximately 2-3m from, the nest box using a small flexible tripod

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and covered the camera body and tripod, except for the lens, with a piece of camouflage cloth. I
took two videos starting early in the morning (between 0600 and 0900), one on day 5-8 and one
at the 10-12 day of the nestling period. Cameras were left in place for approximately three hours
and then collected. Due to battery life and high heat, individual videos ranged in length from 13
to 130 minutes.

Figure 3.1 Image of an urban mountain chickadee nest box taken from a GoPro HERO7 camera.

To increase the sample size, I also included video recordings of parental feedings made
using similar protocols during the 2016 and 2018 field seasons. Teams in those years recorded
approximately 90-minute videos of feeding visits between the hours of 07:35 an 09:39h when
nestlings were 8 or 9 days old. The cameras used were a HD GoPro Hero2 and a HD GoPro
Hero3. The cameras were attached to either the nestbox or a branch of a nearby tree (within ~2-

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3m) with the lens aimed at the nestbox entrance, similar to the protocols I adopted in 2019, but
without camouflaging the cameras.
3.2.2 Data consolidation
Since the data from 2016 and 2018 was based on one video per nest box as opposed to two, I
selected one video from each nest for the 2019 data. From the two videos collected in 2019, I
selected a video from each nest site based on video length and video quality, so that there were
approximately equal numbers of “early” (day 5 to 8) and “late” (day 10-12) videos.
3.2.3 Video analysis
I analysed the videos using BORIS, a free open-source event-logging software program
(Friard and Gamba, 2016). I began scoring videos after excluding the first five minutes of
recording, to account for the time needed to set up the camera and for the birds being disrupted
by human presence. For each video, I noted the number of feeding visits to the nest, which
consisted of observing an adult with food enter the cavity and exit either without food or carrying
a nestling fecal sac for disposal. While scoring the videos I made note of each time a food item
was clearly visible and identifiable. As the cameras were sufficiently distant from the entrance so
as not to disrupt parental activity, it was not possible to identify the feeding parent in most cases,
so all feeding rates are combined male/female visits. Feeding Rate was calculated as the number
of feeding events per hour per chick in the nest.
3.2.4 Frass collection
In order to estimate caterpillar (Lepidopteran larvae) abundance in 2019 I used the frassfall method described by Hajdasz et al.(2019). This method uses large plastic buckets placed
under trees to catch caterpillar frass as it falls from the tree canopy. I constructed the traps out of
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plastic buckets with a 30cm diameter with a concave mesh screen secured to the top of the
bucket. I placed a napkin over the mesh to collect the frass, secured in place with an elastic band.
To ensure drainage I drilled holes in the bottom of each bucket and placed several heavy rocks in
the bucket to keep the buckets upright.
I collected frass at each nest when nestlings were 3-9 and 9-12 days old. I took north,
south, east, and west bearings from each nest and located a tree or large bush 8-10m away from
the nest under which I placed the frass collector. I recorded the time and date of placement and
the time and date that the frass was collected, 4 days after placement. Once collected I dried the
frass in a drying oven at 40°C for 48 hours. After removing dust and debris from the frass sample
I used an analytical balance to get an accurate weight for each sample. I then calculated the
amount of frass in μg/hour.
3.2.5 Data analysis
All Analyses were conducted in R (v 4.3.1, R Development Core Team, 2023) using
RStudio(build 494, 2023-10-16) To assess the effect that urbanization and other factors had on
the Feeding Rate (feeding visits/hour/nestling) and nestling growth rates (as measured by change
in wing chord length between day 6 and day 9 in mm/day, averaged across all chicks in the nest),
I constructed generalized linear mixed models with gamma distributions in R (R package
glmmTMB, Brooks et. al. 2023). I first assessed whether feeding rate and growth rates were
dependent on the number of nestlings in the nest, to determine whether this variable needed to be
controlled in subsequent models. I then tested feeding rates and growth rates against urban/rural
classification and the year of sampling as fixed effects. In both models, I included both the fixed
effects and the interaction term for initial models, then used backwards step-wise removal (P to

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remove >0.1) for all non-significant interaction terms until only significant interactions and/or
the original fixed effects remained in the model.
To further examine the relationship between year and both growth rate and feeding rate I
obtained temperature data on the day of nest observation from the government of Canada website
and prepared models comparing temperature and year as well as temperature and growth rate and
temperature and feeding rate. The temperature data was collected by NAV Canada at Kamloops
airport (YKA). To see if temperature varied between years, the first model was a generalized
linear model with year of sampling as the response variable and maximum daily temperature as
the predictor variable. The other two models were generalized linear models with gamma
distributions and had feeding rate and growth rate as predictor variable with temperature as a
fixed effect and year as a random effect for both models.
To compare the identifiable prey items observed in each video I performed ANOVA
models to compare the percentage of prey that were observable and the percentage of prey that
were lepidopteran between urban and rural environments.
I then created models comparing feeding and growth rate data from 2019 to nest parasite
data and temperature as recorded by a data logger fixed to the lid of the box, as this was the only
year of in which these measures were collected. I used general linear models to compare
Feeding Rates and Growth Rates in 2019 to average daily maximum temperatures at the nest box
and number of blow flies (negative binomial distribution) found in each nest as fixed effects.

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3.3 Results
Overall, we obtained video recordings from 36 nests over three field seasons. Recordings were
taken at 6 urban nests and 7 rural nests in 2016, 4 urban nests and 6 rural nests in 2018, and 4
urban nests and 9 rural nests in 2019.
I found no significant association between the feeding rate (visits to the nest/nestling/hr)
and the number of nestlings in the nest (estimate=-56.65+52.52SE, z= -1.08, p= 0.288), so
number of nestlings was not included as a fixed effect in subsequent models.
When I compared feeding rates to habitat and year, the interaction term was not
significant (2018 p=0.333, 2019 p=0.424) and was removed from the model. There was no
effect of habitat on feeding rate (estimate= -120.27+107.73SE, z= -1.12, p= 0.26), but a
significant effect of year (estimate= 473.45+136.79SE, z= 3.46, p= 0.00054). Feeding rates
were significantly higher in 2016 and 2018 than in 2019 (Figure 3.2).
Next, I compared nestling growth rates to year and habitat, but also added feeding rates
into these models. Similarly, I found that there was no significant association between growth
rate and habitats (estimate= 0.525+0.519SE, z= 1.01, p= 0.315), but a significant effect of year.
Growth Rates were significantly higher in both 2018 (estimate= -4.61+0.77SE, z= -5.93,
p<0.001) and 2019 (estimate= -5.93+0.78SE, z= -7.57, p<0.001) compared to the 2016 Growth
Rate (Figure 3.3). I found no significant association between growth rate and feeding rate
(estimate= -848.24+1305.14SE, z=-0.65, p=0.516).

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3.3.1 Identity of food items
While the majority of feeding visits did not have easily identifiable food items, either due
to the distance of the camera from the nestbox or the position of the arriving parents, all
identifiable food items were arthropods. The majority of identifiable food items were
lepidopteran larvae (64%) compared to other arthropods. Between urban and rural sites, there
was no significant difference between the percentage of feeding visits with visible prey (F=
0.355, p = 0.558) or the percentage of observed lepidoptera larvae (F= 0.138, p= 0.714).
3.3.2 Temperature
I observed differences in maximum daily temperature across years
(estimate=0.097+0.024, t=4.06, p=0.00027). The average maximum daily temperature increased
with increasing year; 2019 had the highest mean temperature and 2016 had the lowest mean
temperature (Figure 3.4). There was no significant association between feeding rate and
maximum temperature (estimate=-1.14X10-5+1.00X10-5, z=-1.129, p=0.26). Similarly, there
was no association between growth rate and maximum temperature (estimate=--0.00039+0.020,
z=-0.773, p=0.44).
3.3.3 Parasite and nest box temperature.
I compared data against micro-climate and parasite measures associated with each nest
that was collected in 2019. I found no effect of maximum temperature (estimate = 13.23+ 25.68,
t=-0.52, p=0.619), or blowfly abundance (estimate= 1.36X10-5+5.62X10-3 t=0.002, p=0.998) on
feeding rates in 2019.

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Similarly, there was no significant association between growth rates and maximum
temperature (estimate = -0.018+0.052 t=-0.34, p=0.741), or blowfly abundance (estimate=-8.56X10-6+7.98X10-4, t=-0.011, p=0.992).
There was no association between feeding rate and the amount of frass
(estimate=5.98+5.02, t=1.19, p=0.264) or difference in frass between habitats (estimate=1.31+0.77, t=-1.71, p=0.12).

Figure 3.2 The feeding rate (trips/hour/chick) in both rural (grey) and urban (white) habitats across the
three years of the study.

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Figure 3.3 The growth rate (mm/day) in both rural (grey) and urban (white) habitats across the three years
of the study.

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Figure 3.4 Temperature in Kamloops as recorded by a government weather station on the day nest watch
videos were taken compared.

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3.4 Discussion
Across three breeding seasons, I found no evidence that urbanization influenced feeding and
growth rates. However, feeding rates were higher in 2016 and 2018 than in 2019 and growth
rates were higher in 2018 and 2019 than in 2016, potentially due to differences in temperature
between years. Most of the prey that I could identify from the video footage were Lepidoptera
larvae and there was no obvious difference in size or type between habitat types. Likewise, I
found no evidence of any impact of urbanization on insect abundance as measured by frass. I
also observed no effect of nest box temperature or ectoparasite abundance on either growth rate
or feeding rate.
In Chapter 2, I show that rural nests had a higher abundance of blow fly larvae than rural
nests. While I did not find that this affected growth rates in the current study, I did find that
urban nests fledge on average one extra chick compared to rural nests (Chapter 2). As a result, I
expected parents in rural nests to engage in compensatory feeding to offset the potential impact
of more abundant parasites on nestling condition, as has been found in other studies (HurtrezBousses et al., 1998). For example, in blue tits (Cyanistes caeruleus) high levels of blowfly and
flea parasitism are associated with increased feeding rates (Tripet and Richner, 1997, HurtrezBousses et al., 1998). Similarly, parasitism by hen fleas (Ceratophyllus gallinae) significantly
increased both begging and feeding rate in great tits (Parus major) (Christie et al., 1996). Unlike
these prior studies I did not observe an association between feeding rate and blowfly abundance
in my study, nor did I find an association between feeding rates and urbanization. This may have
been due to the limited sample size in my study compared with others.
Studies on other urban-settling species, such as great tits, have found higher feeding rates at
nests in urban environments. In these studies, urban areas appeared to be associated with lower
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prey quality, in terms of both nutrient content and prey availability, (Isaksson and Andersson,
2006; Sinkovics et al., 2021), indicating that the higher feeding rate may be a way to compensate
for poor prey quality.
Previous research in our study population found that the mass of insect frass collected from
trees adjacent to nests was higher in rural habitat relative to urban habitat (Hajdasz et al., 2019).
Unlike other studies where decreased frass mass in urban areas was associated with lower
reproductive success in nesting birds (potentially indicating that a lower insect abundance led to
food stress), Hajdasz et al. (2019) found no difference in reproductive success of mountain
chickadees between urban/rural habitats. If there are fewer caterpillars in urban areas, urban pairs
may compensate by feeding poorer quality food items (such as seeds) more frequently, like the
pattern seen in Sinkovics et al. (2021) resulting in a higher feeding rate in urban areas. Hajdasz
et al. (2019) suggested that although the total abundance of frass may have been higher,
differences in caterpillar species composition between habitat types may result in more, but
potentially less nutritious and less preferable caterpillars in rural habitats. Although I could not
identify prey to species, I found little evidence that rural birds fed less caterpillars to their
nestlings, nor that these appeared to differ noticeably in appearance or size. In addition, I found
no difference in frass levels collected under trees between habitat types. While no analysis of
nutrient levels between caterpillars found in either habitat type was done for my study, the
majority of identifiable prey items observed in my study were Lepidoptera larvae irrespective of
habitat type.
One way to potentially elucidate whether prey differs between rural and urban sites may be
to conduct analysis of relative size or nutrient content of prey sampled around nest sites.
Sinkovics et al. (2021) utilized cameras that were placed in a camera box that was integrated

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with nest box allowing them to get much closer images of the prey items and estimate volume of
individual prey items. Isaksson and Anderson (2007) collected caterpillars from great tit
foraging areas and used high pressure liquid chromatography to determine the levels of
carotenoids in the collected caterpillars. If future research on the study population utilized these
methods to better characterize the prey available to Mountain Chickadees it may provide
important information on how both diet and feeding rate differ based on urbanization.
The primary differences I observed in feeding rate and growth rate were due to annual
variation. Given that there were significant differences between the maximum daily temperature
in Kamloops across years, this climatic factor may have influenced feeding and growth rates.
growth rate increased in relation to years with increasing temperature and feeding rate appeared
to decrease in those same years with higher temperatures. Feeding rate can be affected by
temperature in multiple ways; high temperatures may inhibit feeding due to heat stress and low
temperatures can increase the need for food (Garcia-Navas et al., 2012). Cold temperatures have
been noted to increase feeding rates in multiple bird species (Lee et al., 2011). Growth rate can
also be affected by temperature; the growth rate of Gambel’s White-crowned Sparrow
(Zonotrichia leucophrys gambelii) and Lapland Longspur (Calcarius lapponicus) has been
observed to decrease as temperature decreases (Pèrez et al., 2016). The ability to apply
temperature information across years to this study is limited as the only temperature data
available for all three years of sampling is historical data for the whole of Kamloops as opposed
to the microclimate temperatures obtained at the nest boxes in 2019. Since the temperature data
loggers have now been in place for each subsequent field season since 2019, future studies of
feeding rate may have more power to discern subtle effects of micro-climate on feeding and
growth rates. Further studies would be aided by using technology to gather feeding rates or more

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extended and continuous time periods, such as the use of PIT-tagged birds and RFID-equipped
nest boxes (similar to the method used in Garcia-Navas and Sanz, 2012).
Although I hypothesized that increased parasitism in rural nests (Chapter 2) would lead to
increased feeding rates to compensate, I did not find this effect. This could be due to multiple
interactions between urbanization and ecological impacts on Mountain Chickadees effectively
countering one another. For example, if relative prey abundance were higher in rural sites
(Hajdasz et al. 2019), it may have been urban birds that were expected to increase compensatory
feeding. Due to increased nestling condition from reduced parasite loads, this may, however,
have been nullified. The complex interplay of urban impacts may enhance some attributes of
nesting while impacting others, and species that can adjust to these differences may be able to
better adapt to urban environments. To disentangle these interactions, it may be necessary to
collect feeding rate, growth rate, temperature, and ectoparasite data over multiple years, as well
as collect more precise data on prey quality.

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3.5 References
Blair, R. B. (1996). Land Use and Avian Species Diversity Along an Urban Gradient. Ecological
Applications, 6(2), 506–519. https://doi.org/10.2307/2269387
Brooks, M., Bolker, B., Kristensen, K., Maechler, M., Magnusson, A., McGillycuddy, M.,
Skaug, H., Nielsen, A., Berg, C., Bentham, K. van, Sadat, N., Lüdecke, D., Lenth, R.,
O’Brien, J., Geyer, C. J., Jagan, M., Wiernik, B., & Stouffer, D. B. (2023). glmmTMB:
Generalized Linear Mixed Models using Template Model Builder (1.1.8) [Computer
software]. https://cran.r-project.org/web/packages/glmmTMB/index.html
Christe, P., Richner, H., & Oppliger, A. (1996). Begging, food provisioning, and nestling
competition in great tit broods infested with ectoparasites. Behavioral Ecology, 7(2), 127–
131. https://doi.org/10.1093/beheco/7.2.127
Friard, O., & Gamba, M. (2016). BORIS: A free, versatile open-source event-logging software
for video/audio coding and live observations. Methods in Ecology and Evolution, 7(11),
1325–1330. https://doi.org/10.1111/2041-210X.12584
García-Navas, V., & Sanz, J. J. (2012). Environmental and Within-Nest Factors Influencing
Nestling-Feeding Patterns of Mediterranean Blue Tits (Cyanistes caeruleus)—Factores
Ambientales y Sociales que Influyen en los Patrones de Aprovisionamiento de las Crías de
Cyanistes caeruleus. The Condor, 114(3), 612–621. https://doi.org/10.1525/cond.2012.110120
Gold, C. S., & Dahlsten, D. L. (1983). Effects of Parasitic Flies (Protocalliphora spp.) on
Nestlings of Mountain and Chestnut-Backed Chickadees. The Wilson Bulletin, 95(4), 560–
572.
Grundel, R. (1987). Determinants of Nestling Feeding Rates and Parental Investment in the
Mountain Chickadee. The Condor, 89(2), 319–328. https://doi.org/10.2307/1368484
Grundel, R. (1990). The Role of Dietary Diversity, Prey Capture Sequence and Individuality in
Prey Selection by Parent Mountain Chickadees (Parus gambeli). Journal of Animal Ecology,
59(3), 959–976. https://doi.org/10.2307/5025

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Hajdasz, A. C., Otter, K. A., Baldwin, L. K., & Reudink, M. W. (2019). Caterpillar phenology
predicts differences in timing of mountain chickadee breeding in urban and rural habitats.
Urban Ecosystems, 22(6), 1113–1122. https://doi.org/10.1007/s11252-019-00884-4
Harriman, V. B., Dawson, R. D., Clark, R. G., Fairhurst, G. D., & Bortolotti, G. R. (2014).
Effects of ectoparasites on seasonal variation in quality of nestling Tree Swallows (
Tachycineta bicolor ). Canadian Journal of Zoology, 92(2), 87–96.
https://doi.org/10.1139/cjz-2013-0209
Hurtrez-Boussès, S., Blondel, J., Perret, P., Fabreguettes, J., & Renaud, F. R. (1998). Chick
parasitism by blowflies affects feeding rates in a Mediterranean population of blue tits.
Ecology Letters, 1(1), 17–20. https://doi.org/10.1046/j.1461-0248.1998.00017.x
Isaksson, C., & Andersson, S. (2007). Carotenoid Diet and Nestling Provisioning in Urban and
Rural Great Tits Parus major. Journal of Avian Biology, 38(5), 564–572.
Knutie, S. A., Owen, J. P., McNew, S. M., Bartlow, A. W., Arriero, E., Herman, J. M., DiBlasi,
E., Thompson, M., Koop, J. A. H., & Clayton, D. H. (2016). Galápagos mockingbirds tolerate
introduced parasites that affect Darwin’s finches. Ecology, 97(4), 940–950.
https://doi.org/10.1890/15-0119.1
Kurucz, K., Purger, J. J., & Batáry, P. (2021). Urbanization shapes bird communities and nest
survival, but not their food quantity. Global Ecology and Conservation, 26, e01475.
https://doi.org/10.1016/j.gecco.2021.e01475
Lee, J. K., Chung, O.-S., & Lee, W.-S. (2011). Altitudinal Variation in Parental Provisioning of
Nestling Varied Tits (poecile Varius). The Wilson Journal of Ornithology, 123(2), 283–288.
Marini, K. L. D., Otter, K. A., LaZerte, S. E., & Reudink, M. W. (2017). Urban environments are
associated with earlier clutches and faster nestling feather growth compared to natural
habitats. Urban Ecosystems, 20(6), 1291–1300. https://doi.org/10.1007/s11252-017-0681-2
McCallum, D. A., Grundel, R., & Dahlsten, D. L. (2020). Mountain Chickadee (Poecile
gambeli), version 1.0. Birds of the World. https://doi.org/10.2173/bow.mouchi.01

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Meineke, E. K., Dunn, R. R., Sexton, J. O., & Frank, S. D. (2013). Urban Warming Drives Insect
Pest Abundance on Street Trees. PLOS ONE, 8(3), e59687.
https://doi.org/10.1371/journal.pone.0059687
Pérez, J. H., Krause, J. S., Chmura, H. E., Bowman, S., McGuigan, M., Asmus, A. L., Meddle, S.
L., Hunt, K. E., Gough, L., Boelman, N. T., & Wingfield, J. C. (2016). Nestling growth rates
in relation to food abundance and weather in the Arctic. The Auk, 133(2), 261–272.
R Core team. (2023). R: A Language and Environment for Statistical Computing (4.3.1)
[Computer software]. R Foundation for Statistical Computing.
Richner, H., & Tripet, F. (1999). Ectoparasitism and the Trade-Off between Current and Future
Reproduction. Oikos, 86(3), 535–538. https://doi.org/10.2307/3546657
Ruas, R. de B., Costa, L. M. S., & Bered, F. (2022). Urbanization driving changes in plant
species and communities – A global view. Global Ecology and Conservation, 38, e02243.
https://doi.org/10.1016/j.gecco.2022.e02243
Seress, G., & Liker, A. (2015). Habitat urbanization and its effects on birds. Acta Zoologica
Academie Scientarium Hungaricae, 61(4), Article 4.
Simon, A., Thomas, D. W., Speakman, J. R., Blondel, J., Perret, P., & Lambrechts, M. M.
(2005). Impact of Ectoparasitic Blowfly Larvae (Protocalliphora Spp.) on the Behavior and
Energetics of Nestling Blue Tits (Impacto del ectoparásito (Protocalliphora spp.) en la
conducta y energética de pichones de Parus caeruleus). Journal of Field Ornithology, 76(4),
402–410.
Sinkovics, C., Seress, G., Pipoly, I., Vincze, E., & Liker, A. (2021). Great tits feed their nestlings
with more but smaller prey items and fewer caterpillars in cities than in forests. Scientific
Reports, 11(1), Article 1. https://doi.org/10.1038/s41598-021-03504-4
Tripet, F., & Richner, H. (1997). Host Responses to Ectoparasites: Food Compensation by Parent
Blue Tits. Oikos, 78(3), 557–561. https://doi.org/10.2307/3545617

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Van Balen, J. H. (1973). A Comparative Study of the Breeding Ecology of the Great Tit Parus
major in Different Habitats. Ardea, 55(1–2), 1–93. https://doi.org/10.5253/arde.v61.p1

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CHAPTER 4: CONCLUSIONS AND FUTURE DIRECTIONS
4.1 Nest parasitism and compensatory behaviour in mountain chickadee nests.
My goal of this thesis was to investigate how urbanization affects the nest parasites and
consequent parental behaviour of mountain chickadees. In chapter 2 I found that abundance of
blow fly puparia was higher in rural nests, but that flea abundance was more associated with
temperature rather than urbanization. Additionally, I observed that urban nests fledged
approximately one additional chick per nest, which may have been a consequence of reduced
parasitism. When I examined feeding and growth rate I found no evidence that urbanization or
ectoparasite abundance influenced parental feeding or growth rate. This suggests that differences
in ectoparasite levels across habitats don’t necessarily translate to compensatory feeding or
decreased growth rates. I did, however, find that feeding rate was lower and that growth rate was
higher in warmer years.
Prior research at the study site found that adult mountain chickadees did not show evidence
of reduced condition in urbanized landscapes (Marini et al.2017). Further, earlier nesting, higher
dawn chorus song rates, and higher nestling growth rates suggest mountain chickadees may
adapt to urban landscapes (Marini et al.2017). This was somewhat surprising since mountain
chickadees are considered montane conifer specialists and specialist species are often predicted
to be less likely to adapt to urbanization (Blair, 1996; McCallum et. al., 2020). Urbanization
results in meteorological and vegetation changes that can impact birds as well as their prey and
parasites (Seress and Liker, 2015). Based on the parasite release hypothesis (Le Gros et al.
2011)., where species in urban environments may experience increased success due to a
reduction in parasites, I predicted that urban nests would have fewer nest ectoparasites and

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fledge more young than rural nests. I found that urban nests had less blow fly puparia and
fledged more young than rural nests which supports the parasite release hypothesis (Chapter 2).
However, flea abundance was associated with temperature rather than habitat type; cooler
temperatures predicted more fleas in nests.
Since blow flies are free living as adults I proposed that the reduction in vegetation
associated with urbanization might reduce the abundance of adult blow flies which in turn would
reduce the number of puparia in urban nests. Adult Protocalliphora blow flies feed on pollen
from wildflowers and fruit (Bennett and Whitworth, 1991), which may be reduced in urban
areas, impacting the ability of adult blowflies to find food and reproduce. As I found more fleas
in 2020, the cooler of the two years, I proposed that lower temperatures may favour the survival
of fleas at the study site. Experimental heating of nests has been shown to reduce flea abundance,
but humidity may also be an important determining factor in flea survival (Castano-Vasquez et
al., 2021). While I found no association between the abundance of either ectoparasite I did find
that urban nests fledged one more chick per nests. Finding no obvious impact of parasitism on
nestlings is not uncommon and it has been suggested that parental and nestling behaviour may
mask the impact of parasitism (Goodenough et. al., 2011). Increased provisioning by parents can
mask the cost of parasitism on nestlings and transfer the costs of parasitism to the parents
(Goodenough et. al., 2011).
Although I predicted that rural areas would have higher feeding rates based on the idea of
compensatory feeding, I found no evidence that urbanization or ectoparasite abundance impacted
either feeding or growth rate. This result may be due to the limited sample size in this chapter or
the interaction between multiple urbanization impacts. Higher feeding rates in urban
environments have been observed in other urban settling species and have been proposed as a

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way to compensate for poorer prey quality (Isaksson and Andersson, 2006; Sinkovics et al.,
2021). While I found no difference in the abundance of insects as measured by frass between
habitat types or an obvious difference in the composition of prey brought to the nest, prior
research at the study site indicated that rural sites had higher frass abundance than urban sites,
suggesting a greater abundance of prey at rural sites (Hajdasz et al., 2019). The equal feeding
rates at urban and rural sites may be due to birds engaging in two different forms of
compensatory feeding with urban birds compensating for food quality or quantity and rural birds
compensating for parasitism.
While these results provide important information on the breeding ecology of mountain
chickadees additional research is needed to fully discern how urbanization affects parasitism and
feeding rate in mountain chickadees. Urban adapted species may be thought of as “making the
best of a bad situation” in that they are still able to find food and nest sites in urban landscapes as
opposed to being totally excluded (Seress and Liker , 2015). There may, however, be a more
nuanced mix of benefits and challenges for urban settling birds to overcome. My results in
Chapter 2 show some evidence of a clear benefit to settling in urban environments, a reduction in
ectoparasites. If urban environments are associated with reduced parasitism they may hold
advantages for species with sufficient flexibility of behavioural and life history traits.
4.2 Future Directions
Temperature and microclimate were important across all of the topics in this thesis. Since 2019
Onset HOBO Pendant Wireless Temperature and Light Data Loggers (model MX2202) have
been placed on each active nest box at the study site. While these provide important information
on the microclimate of the nest, additional microclimate information, such as temperature and

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humidity within the nest box would help to further decipher what controls the abundance of
ectoparasites in mountain chickadee nests.
Obtaining an accurate measure of the temperature within a nestbox is slightly more
complicated than obtaining the temperature outside of the nest box. In order to not disturb the
nesting birds the data logger or probe needs to be camouflaged and handling the data logger to
obtain data should be avoided. Probes can be camouflaged to match the nest material as much as
possible or they can even be made to resemble eggs (Weidinger, 2006; Hund et al., 2022). The
existing HOBO data loggers could likely be modified for use as in-nest temperature loggers by
camouflaging them and attaching them to the wall of the nest box below the upper boundary of
the nest cup, but new data loggers, such as TS-100 temperature-humidity data loggers, may be
needed to measure humidity within the nestbox.
Nest material is another important factor of the nest environment that affects nest
ectoparasites. Aromatic plants are often incorporated into the nests of several species of bird and
they are thought to reduce parasites in the nest (reviewed in Scott-Baumann and Morgan, 2015).
When incorporated into nest material, anthropogenic material, like tobacco obtained from
discarded cigarettes, has been shown to be associated with a lower abundance of nest
ectoparasites (Suárez-Rodríguez et al., 2013; Hanmer et al., 2017). Vegetation changes between
urban and rural environments could also lead to urban birds including different, possibly more
aromatic, plant material in their nests in addition to gathered anthropogenic material. Identifying
the varieties of plants as well as the types of anthropogenic material included in mountain
chickadee nests could provide important information on how urbanization affects nest
construction and how that in turn affects nest ectoparasites.

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To further assess nestling provisioning rate at the study site PIT tag readers could be used to
obtain data over a longer period of time. All of the parent birds at the study site are now PIT
tagged and RFID readers, similar to the ones used at the study site in the past to assess visitation
rate at bird feeders, could be attached to nest boxes. A copper antenna (similar to that used in
Stanton et al., 2016) would be attached to the nestbox entrance and the main body would be
attached to the bottom of the nest box. While the data obtained from this would need to be
compared to video monitoring data to ensure it truly represented feeding rate, it would provide
data over a much longer timescale than video monitoring.
While I was able to obtain feeding rate of the video footage, I captured I was only able to
obtain anecdotal information on the prey brought to the nest due to the distance of the camera
from the nest box entrance making detailed identification of prey and quantification of size
difficult. Since a better characterization of the prey brought to the nest would be useful in
determining prey quality across habitat types, future studies should attempt to obtain closer
footage. Having the camera closer to the nest box may initially disturb the birds, but attaching
the camera mount alongside a dummy camera at the beginning of the breeding season should
help minimize this by allowing birds to acclimate. Once the birds are acclimated, videos could be
taken at the desired nestling age and then prey size and identity could be determined by
analyzing the video footage using the methods outlined in Sinkovic et al., (2018). Other aspects
of prey quality, such as carotenoid content, could be assessed by collecting potential prey items
from vegetation with the foraging range around each nest box and analyzing the nutrient content
in a laboratory setting.

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4.3 References
Hanmer, H. J., Thomas, R. L., Beswick, G. J. F., Collins, B. P., & Fellowes, M. D. E. (2017).
Use of anthropogenic material affects bird nest arthropod community structure: Influence of
urbanisation, and consequences for ectoparasites and fledging success. Journal of
Ornithology, 158(4), 1045–1059. https://doi.org/10.1007/s10336-017-1462-7
Hund, A. K., McCahill, K. A., Hernandez, M., Turbek, S. P., Ardia, D. R., Terrien, R. C., &
Safran, R. J. (2022). An Experimental Analysis of the Fine-Scale Effects of Nest Ectoparasites
on Incubation Behavior (p. 2022.07.09.499424). bioRxiv.
https://doi.org/10.1101/2022.07.09.499424
Scott-Baumann, J. F., & Morgan, E. R. (2015). A review of the nest protection hypothesis: Does
inclusion of fresh green plant material in birds’ nests reduce parasite infestation?
Parasitology, 142(8), 1016–1023. https://doi.org/10.1017/S0031182015000189
Seress, G., & Liker, A. (2015). Habitat urbanization and its effects on birds. Acta Zoologica
Academie Scientarium Hungaricae, 61(4), Article 4.
Sinkovics, C., Seress, G., Fábián, V., Sándor, K., & Liker, A. (2018). Obtaining accurate
measurements of the size and volume of insects fed to nestlings from video recordings.
Journal of Field Ornithology, 89(2), 165–172. https://doi.org/10.1111/jofo.12248
Stanton, R. L., Morrissey, C. A., & Clark, R. G. (2016). Tree Swallow (Tachycineta bicolor)
foraging responses to agricultural land use and abundance of insect prey. Canadian Journal of
Zoology, 94(9), 637–642. https://doi.org/10.1139/cjz-2015-0238
Suárez-Rodríguez, M., López-Rull, I., & Macías Garcia, C. (2013). Incorporation of cigarette
butts into nests reduces nest ectoparasite load in urban birds: New ingredients for an old
recipe? Biology Letters, 9(1), 20120931. https://doi.org/10.1098/rsbl.2012.0931

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Weidinger, K. (2006). Validating the use of temperature data loggers to measure survival of
songbird nests. Journal of Field Ornithology, 77(4), 357–364. https://doi.org/10.1111/j.15579263.2006.00063.x

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