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Glob Change Biol. 2023;00:1–12.
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1wileyonlinelibrary.com/journal/gcb
Received: 14 Februar y 2023
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Revised: 18 August 2023
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Accepted: 24 August 2 023
DOI : 10.1111/gcb .16935
RESEARCH ARTICLE
Phenotypic signatures of urbanization? Resident, but not
migratory, songbird eye size varies with urban- associated light
pollution levels
Todd M. Jones1,2,3 | Alfredo P. Llamas1 | Jennifer N. Phillips1,4
This is an op en access arti cle under the ter ms of the Creative Commons Attribution-NonCommercial License , which permits use, dis tribu tion and reprod uction
in any medium, provided the original work is properl y cited an d is not use d for comm ercial purposes.
© 2023 The Authors . Global Change Biology published by John W iley & Sons Ltd.
1Depar tment of Life Sciences, Texas A &M
University- San Antonio, S an Antonio,
Texas, USA
2Migratory Bird Center, Smithsonian's
Nationa l Zoo and Conser vation B iolog y
Instit ute, Washi ngton , DC, USA
3Illinois Natura l Histor y Survey, Prairie
Research Insti tute, University of Illi nois at
Urbana- Champaign, Champaign, Illinois,
USA
4School of the Environment , Washing ton
State Universit y, Pullman , Washing ton,
USA
Correspondence
Todd M. Jones , Department of Life
Science s, Texas A&M University- San
Antonio, San Anto nio, TX , USA.
Email: jonestm@si.edu
Abstract
Urbanization now exposes large portions of the earth to sources of anthropogenic
disturbance, driving rapid environmental change and producing novel environments.
Changes in selec tive pressures as a result of urbanization are often associated with phe-
notypic divergence; however, the generality of phenotypic change remains unclear. In
this study, we examined whether morphological phenotypes in two residential species
(Carolina Wren [Thryothorus ludovicianus] and Northern Cardinal [Cardinalis cardinalis])
and two migratory species (Painted Bunting [Passerina ciris], and White- eyed Vireo
[Vireo griseus]), differed between urban core and edge habitats in San Antonio, Texas,
USA. More specifically, we examined whether urbanization, associated sensory pollu-
tion (light and no is e) and brightne ss (op en, bri ght areas cau se by anthrop og enic land use)
influenced measures of avian body (mass and frame size) and lateral eye size. We found
no differences in body size between urban core and edge habitats for all species except
the Painted Bunting, in which core- urban individuals were smaller. Rather than a direct
effect of urbanization, this was due to differences in age structure between habitats,
with urban- core areas consisting of higher proportions of younger buntings which are,
on average, smaller than older birds. Residential birds inhabiting urban- core areas had
smaller eyes compared to their urban- edge counterparts, resulting from a negative as-
sociation between eye size and light pollution and brightness across study sites; not ab ly,
we found no such association in the two migratory species. Our findings demonstrate
how urbanization may indirectly influence phenotypes by altering population demo-
graphics and highlight the importance of accounting for age when assessing factors driv-
ing phenot ypic change. We also provide some of the first evidence that birds may adapt
to urban environments through changes in their eye morphology, demonstrating the
need for future research into relationships among eye size, ambient light microenviron-
ment use, and disassembly of avian communities as a result of urbanization.
KEYWORDS
body size, demographics, eye size, phenotypic divergence, sensory pollution, songbirds,
urbanization
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JONES e t al.
1 | INTRODUCTIO N
The pervasive growth of urbanization now exposes large portions
of the earth to sources of anthropogenic disturbance, driving rapid
environmental change and creating habitats that have never before
existed (Seress & Liker, 2015). Responses of organisms to urban-
ization can serve as important models for evolutionary ecologists,
as phenotypic divergence may be evident between populations
found in urban and more natural systems (Caizergues et al., 2018;
Charmantier et al., 2017; Marzluff, 2001), thus providing novel op-
portunities to investigate eco- evolutionar y processes in the face of
rapid environmental change. Indeed, research has demonstrated that
urbanization can act as an important ecological filter through which
species and individuals with particular phenotypes are favored,
leading to changes in community composition (Marzluff, 2001;
McKinney, 2002; Shochat, 200 4; Shochat et al., 2006, 2010) and in-
traspecific phenotypic traits (Hantak et al., 2021; Iglesias- Carrasco
et al., 2017; Martin & Sheridan, 2022). Given the projected impacts
of urbanization toward future biodiversity (Ceballos et al., 2015;
Elmqvist et al., 2013; McDonald et al., 2008; Vimal et al., 2012),
understanding the phenotypic responses of organisms to human-
altered habitat s is important for improv ing our un der st anding of po-
tential drivers of species persistence and loss (Dominoni et al., 2020;
Isaksson et al., 2018).
In birds, research in urban ecology has revealed many cases of
phenotypic divergence between conspecifics in urban and more
na t u r al h abi tat s, inclu din g bu t no t li mite d to a ran ge of mo r p h o log-
ical, physiological, and behavioral traits (e.g., Corsini et al., 2022;
Jones et al., 2010; Liker et al., 2008; Smith et al., 2021). One trait
of particular interest to ecologists has been body size. Body size
is an integrator trait linked with many ecological characteris-
tics of organisms (Brown & Maurer, 1986; Gould, 1966; Hantak
et al., 2021), and as such, understanding factors mediating body
size has been a central goal in ecology for more than a half cen-
tury (Peters, 198 3). Ur baniz ation is though t to influenc e bo dy size
of birds and other endotherms through several, non- mutually ex-
clusive means. First, urban areas are generally warmer than sur-
rounding areas due to a heat accumulation phenomenon known
as the urban heat island (UHI) effect, caused by urban construc-
tion and other human activities (Yang et al., 2016). If, under Berg-
man's rule, species tend to decrease in size in association with
higher temperatures (Bergmann, 18 47; Salewski & Watt, 2017),
then conspecifics inhabiting urban heat islands are predicted to
have smaller body size than those in more natural areas. Second,
urban areas are often associated with increases in the abundance
and availability of food and water. Access to reliable, high- energy
resources may allow for greater growth rates and larger body
sizes in urban individuals (“resource rule”; McNab, 2010). Third,
research by Schmidt and Jensen (2005) suggests that with land-
scape fragmentation caused by urbanization, organisms should
follow the “island rule” (Lomolina, 1985); smaller species should
increase in body size, while larger species should decrease (e.g.,
Clegg & Owens, 2002). Finally, urbanization often leads to noisier
habitat s, which should favor vocalizations at higher frequencies
(Badyaev et al., 2008). As the mass of vibrating structures is as-
sociated with both vocal frequency and overall body mass (Ryan
& Brenowitz, 198 5), this suggests that nosier urban environment s
may favor smaller individuals through more efficient vocalizations
(Ortega, 2012). While each of these hypotheses has distinctive
predictions for changes in avian body size, past evidence for
and against each hypothesis has been mixed (reviewed in Sepp
et al., 2017 ), highlighting the need for further examination of this
important trait in the context of urbanization.
Besides body size, an overlooked but potentially important phe-
notype for urban environment s is eye size. For birds and many other
animals, eyes represent the primary external anatomical structure to
sense light (Ausprey, 2021; Hart et al., 2000), and avian species may
show an evolutionary response to light via increases or reductions
in eye size (Ausprey et al., 2021). Larger eyes collect more light and
expand perceptual range through improved visual acuity and sen-
sitivit y to contrast (Thomas et al., 2004). However, this comes at a
cost, as larger eyes are more susceptible to overexposure or glare,
which may impac t their ability to transverse their environment, for-
age, and detect predators (Fernandez- Juricic & Tran, 2007; Martin
& Katzir, 2000). For instance, birds transitioning to extremely bright
environments, which are common in urban and anthropogenically
modified landscapes, have been experimentally shown to reduce
foraging bouts and anti- predator behaviors (Fernandez- Juricic &
Tra n , 2007). Thus, larger- eyed species may be deterred from oc-
cupying or making movements across brightly lit environments
(Martinez- Ortega et al., 2014). Ultimately, such research suggests
that eye size is a functional trait that is integral for determining avian
niches and predicts sensitivity to light (Ausprey, 2021), with birds
with larger eyes (relative to body size) occupying darker microen-
vironments and being more sensitive to brightly lit environments
(Ausprey, 2021; Martinez- Ortega et al., 2014). Light may there-
fore be a key factor driving avian responses in urban areas, owing
to the brighter conditions created by human construction, reflec-
tive surfaces, landscape fragmentation, and artificial light at night
(Dominoni et al., 2016). Also, if urban areas are brighter and eye size
determines a bird's ability to cope with brighter environments, then
conspecifics are predicted to have smaller eyes in urban areas com-
pared to those in more natural habitats. However, to our knowledge,
no study to date has examined potential differences in avian eye size
between urban and more natural habitats.
Here, we investigated the influence of urbanization on the
phenotypic traits of residential and migratory songbirds breed-
ing in San Antonio, Texas, USA. More specific ally, the objective
of our study was to determine whether there were intraspecific
differences in body size and eye size between birds inhabiting
urban- edge (more natural) and urban- core habitats across the city
(hereafter referred to as “core” and “edge” areas). Fur thermore, we
examined whether differences in noise and light pollution were
associated with songbird body and eye size respectively. Notably,
we incorporated breeding migratory species into the study as they
may only be present in urban areas for part of their annual cycle
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JONES et al.
(e.g., breeding season) and inhabit natural areas during the rest of
the year. Thus, such species may be subjec t to conflicting selec-
tive pressures of urban and natural areas, providing an interesting
contrast to residential species that inhabit and are subject to the
selective forces in urban areas year- round. Based on this and find-
ings from previous studies (e.g., Ausprey, 2021; Liker et al., 2008),
we pre di cted: (1) th at bo dy siz e and eye size of bir ds inhabiti ng core
areas will be smaller than those inhabiting edge areas; (2) that avian
body size and eye size would be smaller in noisier, brighter, and
more light polluted areas, respec tively; and (3) that differences in
body size and eye size between core and edge conspecifics will be
smaller or absent in migratory species.
2 | MATERIALS AND METHODS
2.1 | Study sites
Data (Jones et al., 2023) were collec ted in 2022 at five edge sites
(Texas A&M University- San Antonio Campus, Mitchell Lake Audu-
bon Center, Government State Canyon Natural Area, Medina River
Natural Area, and Eisenhower Park) and four core sites (Phil Hard-
berger Park, McAllister Park, Salado Creek, and the San Antonio
River) across San Antonio, Texas, USA. Sites were classified as core
or edge areas based on the amount of impervious or “built” land
cover (e.g., roads, buildings, residential and business areas) present
in a 3.22 km (2 mile) radius of each study site. Using high resolu-
tion 2022 imagery from Google Earth Pro, we manually created
polygons using the polygon tool to mark impervious cover, using
the total area to determine the percentage of cover (e.g., Phillips
et al., 2018) within the circle around the site (Figure 1). We consid-
ered sites to be edge habitats if the surrounding area had <50% im-
pervious cover, while those over 50% were considered core areas.
Notably, our core areas can be considered urban “islands”, as they
were generally surrounded by various sources of impervious cover,
while our edge areas were often connected or adjacent to more
contiguous, non- impervious cover, such as agricultural farms or
rangelands.
2.2 | Environmental measurements
To obtain estimates of noise pollution for each site, we utilized sound
pressure level readings taken at nests or known territories found and
monitored across each study site as part of a larger concurrent study
in the San Antonio area. We chose to sample nest sites and observed
territories rather than banding sites, as nest sites and territories were
more evenly spread out across each study site. We stood next to each
nest and recorded A- weighted continuous noise levels (LAeq; dB re
20 μPa) over a 4 min period using a t ype 1 Larson- Davis 831 sound
level meter with a 20 ms sampling rate; repositioning the meter's mi-
crophone in each cardinal direction after each minute of recording
(Brumm, 2004; Phillips et al., 2020). Noise samples were taken during
morning (sunrise to noon) or evening hours (4– 8 p.m.), when birds were
the most active and traf fic is heaviest to best approximate the sound-
scapes birds experienced. If sudden irregular noises occurred, such as
people talking or moving at close range, or wind above Beauford cat-
egory 2, the recording was halted and resampled at a different time or
date. To estimate light pollution for each site we used data from the
online, public database ‘light pollu tionm ap.info’ (Stare, 2023). Using the
most recent data option ( VIIRS 2021), we sampled measures of light
pollution (10−9 W/c m2*sr ; SI ra di ome tr y unit for rad ian ce) even ly acr oss
each study site, with a consistent number of points sampled per unit
area (1 point per 0.1 km2). Sampled point s were averaged to provide
an overall estimate of light pollution per site. As this metric primarily
concerns light pollution at night, we developed a second metric for an
es ti mate of “lig ht ” dur in g th e da y. Usin g th e sa me tech ni qu e we use d to
estimate impervious cover surrounding sites, we determined the pro-
po rti on of op en, bri gh tly lit are as on ea ch st ud y site— a met ric we ca ll ed
“brightness.” Additionally, to provide more insight into potential find-
ings , we esti ma ted mea n te mpe rat ur es at each site , us in g dat a fr om the
online, public database ‘PRISM’ (PRISM Climate Group, 2023). We too k
an average value of mean annual temperature over the past 5 years
for each site. Environmental characteristics for our study sites can be
found in Table S1.
We examined whether there were differences in light pollu-
tion, brightness, noise pollution, and mean temperature between
urban- edge and urban core sites using general linear models (Proc
FIGURE 1 Example of an (a) urban-
edge and (b) urban- core study site in San
Antonio, Texas, USA. The yellow circle
delineates a 3.22 km (2 mile) radius circle
placed around each site, with polygons
(white shaded areas) used in Google
Earth Pro to determine the percentage
of impervious or “built” cover (e.g., roads,
buildings, residential and business areas)
in the surrounding area.
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4
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JONES e t al.
Glm: SA S Institute, 199 0). Barring one outlier site (Texas A&M
University- San Antonio Campus), urban- core sites were more light
polluted (F = 10.29, p = .018) and brighter (F = 4.44, p = .080) than
urban- edge areas. Light pollution and brightness were highly cor-
related across sites (r = .96), suggesting that sites with greater light
pollution also had more open, brighter areas during the day result-
ing from anthropogenic land use. Unexpectedly, though urban- edge
sites exhibited a greater range of noise pollution, on average they did
not differ significantly from urban- core areas (F = .95, p = .363). Sim-
ilarly, urban- edge sites exhibited a greater range of mean tempera-
tures, but did not differ significantly from urban- core areas (F = .25,
p = .632). Mean temperature also appeared confounded by latitude,
with southern sites generally having warmer temperatures— though
we note at the same latitude, temperatures appear to increase with
closer proximity to downtown San Antonio, suggesting a heat island
effect; this also suggest s greater resolution data may be needed to
detect and test for this effect. For these reasons, we did not include
temperature in our analyses of factors potentially driving changes
in body size.
Given the relative abundances of potential species at each site,
we chose to focus on two residential and two migratory species for
which we could acquire adequate samples sizes to provide a com-
pelling comparison between urban- edge and core habitats. For res-
idential species, we focused on the Northern Cardinal (Cardinalis
cardinalis) and Carolina Wren (Thryothorus ludovicianus), while our
two focal migratory species were the Painted Bunting (Passerina
ciris), and White- eyed Vireo (Vireo griseus) (hereafter also referred
to as cardinal[s], wren[s], bunting[s], and vireo[s], respectively). In
addition to sample size, our residential species were chosen as they
appear to be adapted to urban life, often inhabiting urban areas in
higher densities than more rural habitats (e.g., Rodewald et al., 2011).
Similarly, we chose our migratory species because they actively use
and breed at both urban- edge and urban- core habitats in San An-
tonio. Thus, these four species experience urban habitats during a
significant propor tion of their life histories, and have the potential to
exhibit phenotypic divergence in response to selective pressures of
urban environments.
From March to July, we captured a total of 502 breeding indi-
viduals of these species (Table 1) in mist nets by luring them in with
conspecific playbacks, mobbing calls, or flushing them off nests.
We primarily used conspecific playback to target specific male in-
dividuals, and switched to mobbing calls when that did not work;
we also capture incubating females by flushing them from the nest.
Upon capture, each bird was individually banded, aged, sexed, and
measured for different morphologies including tarsus leng th, wing
length, tail leng th , and lateral eye widt h (we repl icated eye measure-
ments from Ausprey, 2021; Ausprey et al., 2021). After sampling,
each bird was subsequently released back into their habitat. All
capture and handling protocols were approved by A&M- SA IACUC
Protocol 2021- 05, USGS Bird Banding Laboratory Permit #24294,
Texas Parks and Wildlife Depar tment Permits # SPR- 0522- 086, and
in coordination with City of San Antonio Parks and Recreation De-
partment and San Antonio River Authority.
2.3 | Statistical analyses
To examine dif ferences in body and eye size between habitat types
(core vs. edge) and in association with continuous sensory pollution
measurements (noise, light, brightness), we first defined our meas-
urements of interest. Mass is often used in comparative and experi-
mental studies examining changes in body size (reviewed in Ashton
et al., 2000; Meiri & Dayan, 20 03). However, mass can vary in birds
dep en ding on the st age of their life cycles , breeding seaso n, how much
parental care they provide, and even the time of day they are weighed
(e.g., Cox & Cresswell, 2014 ; Lange & Leimar, 2004; Rands et al., 2006).
Th us , in addi ti on to ma ss, we exam ine d bo dy size in the contex t of each
bird's body frame. To do this, we used a principal components analysis
(PCA) to reduce the dimensionality of our other morphological meas-
urements (wing length, tail length, and tarsus length) down to a single,
overarching variable, which we refer to as “frame size.” Frame size was
calculated separatel y for each species, and in the case of the Northern
Cardinal, each sex (see reasoning below), with each variable explain-
ing >44.00% of the variation in morphologies (eigenvalues >1.30)
(Table 2). We used our measurements of lateral eye size as an estimate
of eye size, which should be linked to the functionality of avian eyes
with respect to brightness (Ausprey, 2021; Ausprey et al., 2021).
We exa m ine d dif fer ence s in bo d y and eye si ze be t we en cons p eci f-
ics in edge an d core habitat s and in relatio n to sensor y pollution using
generalized linear mixed models (Proc Glimmix, SAS Institute, 199 0).
Analyses were conducted separately for each species and response
variable. We examined the effect of urbanization on body size using
mass or frame size as the response variable, and habitat type (edge
vs. core), noise pollution, and their additive effects as independent
variable(s). Similarly, we conducted models with eye size as the re-
sponse variable and habitat t ype, light pollution, brightness, and their
additive effects as independent variables; we did not include light
pollution and brightness in the same model due to multicollinearity
TAB LE 1 Names, urban- edge and core samples sizes for, and
migrator y strategy of four focal songbird species in San Antonio,
Texas, USA, 2022.
Focal species Scientific name
Alpha
code
#
Edgea
#
CorebMigratory?
Carolina Wren Thryothorus
ludovicianus
CARW 21 68 No
Northern
Cardinal
(Female)
Cardinalis
cardinalis
NOCA 50 35 No
Northern
Cardinal
(Male)
Cardinalis
cardinalis
NOCA 54 66 No
Painted
Bunting
Passerina ciris PABU 76 35 Ye s
White- eyed
Vireo
Vireo griseus WEVI 44 53 Yes
aSample size of birds capture in more natural, urban- edge habitat s.
bSample size of birds capture in heavily urbanized, urban- core habitats.
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JONES et al.
(r = .964). For each model, we also included study site as a random
effect to account for potential site- specific features that may cause
non- independence of avian phenotypes within sites. Additionally, for
each series of models (i.e., body mass, frame size, eye size) we also in-
cluded an intercept only model to serve as a constant (null) model. For
the Northern Cardinal, we conducted separate analyses for males and
females, as males were generally heavier and larger with respect to
wing, tarsus, and tail. Only measurements for male Painted Buntings
were included in the dataset given the low sample sizes for females
(n = 6), and like cardinals, male buntings were generally heavier and
larger with respect to wing, tarsus, and tail. We pooled males and fe-
males in each of the remaining species, as males and females look the
same and we captured individuals that could not be sexed (e.g., cap-
ture wit h no pla yb ack or with a mob bi ng ca ll and they ha d no bree di ng
condition or the presence of partial brood patches in wrens).
To examine hypotheses on the impacts of urbanization on song-
bird morphology, we used these sets of a priori models in an informa-
tion theoretic approach. Specifically, we ranked models in each series,
per species, using Akaike's information criterion adjusted for small
sample sizes (AICc; Burnham & Anderson, 2002) to determine which
variable(s) best explained variation in morphologies in each species.
We then based our inferences for each variable on whether models
were competing (within 2 delta AICc) wi th th e nu ll mo de l and 85% con-
fidence intervals of coefficients overlapped zero (Arnold, 2010 ).
3 | RESULTS
3.1 | Frame size and body mass
Our PCA analyses produced frame size variables for each species in
which wing, tail, and tarsus length were all positively loaded (Table 2).
The frame size factor explained 48.72% of morphological variation in
the Carolina Wren (eigenvalue = 1.462), 55.34% in female Nor thern
Cardinals (eigenvalue = 1.660), 49.78% in male Northern Cardinals (ei-
genvalue = 1.493), 49.58% in the Painted Bunting (eigenvalue = 1.487),
and 44.4% in the White- eyed Vireo (eigenvalue = 1.324).
For four of the five focal species and sexes, body mass was best
explained by the null model, indicating no effect of noise pollution and
no difference in body mass between edge and core habitats (Table S2;
Figure 2a); note that for female cardinals, models with noise and the
combination of noise and site type ranked above the null model, but
confidence intervals for noise overlapped zero. The one exception
was in the Painted Bunting, in which body mass was best explained
by and negat ive ly associated wit h noise pollution (β = −.037, SE = 0.016,
85% CI = −0.060 to −0.129), such that heavier buntings were caught in
less noise polluted sites. Similarly, for four of the five focal species and
sexes, frame size was best explained by the null model, indicating no
effect of noise pollution and no difference in frame size between edge
and core habitats (Table S3; Figure 2b). Buntings were again the excep-
tion, in which frame size was best explained by the additive effects of
noise and site type. Bunting frame size was negatively associated with
noise pollution ( β = −.030, SE = 0.016, 85% CI = −0.053 to −0.007) and
bunt ing s had significantly small er fr ame sizes in core compared to edge
areas (β = −.654, SE = 0.325, 85% CI = −1.299 to −0.182; Figure 2b).
3.2 | Post- hoc analyses on frame and body size in
Painted Buntings
A post- hoc analysis on the Painted Bunting suggested that variation
in body size among sites may be a result of differences in demo-
graphics (i.e., age structures) between edge and core areas. A general
linear model (Proc Glm, SAS Institute 1990) with the propor tion of
second year (SY; younger) buntings as the response variable (by site)
and habitat type (edge vs. core) as the independent variable showed
significantly more younger birds in core areas ( β = .408, SE = 0.129,
85% CI = 0.104 to 0.712; Figure 3)— the overall ratio of after- second-
year (ASY; older) to SY buntings was 6:1 in edge habitats compared
to 1:2 in core habitats. Furthermore, general linear models (Proc Glm,
SAS Institute 1990) with frame size or mass as the response vari-
able and age as the independent variable found that ASY males were
significantly larger than SY males (frame size: β = .80 8, SE = 0.190,
95% CI = 0.431 to 1.185; mass: β = .531, SE = 0.189, 95% CI = 0.156
to 0.906), suggesting that the presence of more, older males in edge
areas may be driving the trend. Consequently, we repeated our
analyses on the bunting, this time accounting for the confounding
influence of age by including it as a covariate. Though noise pollution
and site type were the top predictors for both mass and frame size in
our age controlled models (Table S4), body mass and frame size did
not differ between urban- edge and core areas (frame size: β = −.329,
SE = 0.286, 85% CI = −0.743 to 0.086; mass: β = .032, SE = 0.318,
85% CI = −0.429 to 0.49). However, we did find the same negative
association between noise pollution and parameters of body size
(frame size: β = −.031, SE = 0.014, 85% CI = −0.051 to −0.010; mass:
β = −.032, SE = 0.017, 85% CI = −0.056 to −0.008).
TAB LE 2 Principal component analyses of morphological
measurements reflecting frame size of songbirds capture in San
Antonio, Texas, USA, 2022.
PCA analyses
Species Eigenvalue
Variance
explained
Loadings
Wing Tail Tarsus
Carolina
Wren
1.634 54.46% 0.916 44 0.8100 8 0.370 94
Northern
Cardinal
(Female)
1.660 55.3 4% 0. 84947 0. 8 0961 0.53199
Northern
Cardinal
(Male)
1.493 49.7 7% 0.86731 0.82395 0 .24921
Painted
Bunting
1.487 4 9.58 % 0.8714 4 0.82757 0. 20774
White- eye
Vireo
1.324 44 .14% 0. 84224 0.6 5511 0.43097
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6
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JONES e t al.
3.3 | Eye size
Eye size in the Painted Bunting and White- eyed Vireo were best
explained by the null model, indicating no effect of light pollution,
brightness, and no difference in eye size between edge and core
ha bi t at s (Table S5; Figure 2c). In the Carolina Wren, eye size was best
explained by light pollution, but we also found a significant effect
of brightness and site type, which were competing models. Wren
eye size was negatively associated with light pollution (β = −.007,
SE = 0.004, 85% CI = −0.013 to −0.002; Figure 4a) and brightness
FIGURE 2 Comparisons of (a) body
mass, (b) frame size, and (c) lateral eye size
between urban- edge and core habitats
for four species breeding across nine
study sites in San Antonio, Texas, USA ,
2022. Asterisks denote occasions where
morphologies were significantly different
between the two habitat t ypes.
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JONES et al.
(β = −.525, SE = 0.284, 85% CI = −0.937 to −0.113), and wrens in-
habiting core areas had significantly smaller eyes than their edge
counterparts (β = −.170, SE = 0.108, 85% CI = −0.3263 to −0.014).
Based on model selection, we found the same trends in male North-
ern Cardinals, in which eye size was negatively associated with light
pollution (β = −.008, SE = 0.003, 85% CI = −0.011 to −0.00 4) and
brightness (β = −0.540, SE = 0.20 4, 85% CI = −0.835 to −0.244), and
males inhabiting core areas has significantly smaller eyes (β = −.144,
SE = 0.062, 85% CI = −0.011 to −0.00 4). Notably, eye size in female
cardinals was best explained by brightness, in which there was
a negative association (β = −.578, SE = 0.331, 85% CI = −1.058 to
−0.0968); light pollution was a competing model and was also nega-
tively associated with eye size. However, a competing model was the
null model (within 2 delta AICc), suggesting no effect of light pollu-
tion on female eye size.
We suspected that the findings on female cardinals may be a
result of a lack of statistical power due to sample sizes, particularly
given that an effect of light pollution was found in Carolina Wrens,
where males and females were pooled. Thus, we conducted a post-
hoc analysis in which we pooled sexes and re- ran our analyses on light
pollution and eye size in c ardinals. In line with findings on the Caro-
lina Wren, cardinal eye size was best explained by light pollution and
brightness (difference of 0.07 AICc between the models; Table S6),
both of which were ranked >2 AICc above the null model. We also
foun d a neg at i ve ass o ci ati on betwe en ca rd ina l ey e si ze and li gh t pol lu-
tion (β = −.007, SE = 0.004, 85% CI = −0.010 to −0.003; Figure 4b) and
brightness (β = −0.523, SE = 0.202, 85% CI = −0.814 to − 0.231) when
sexes were pooled. However, unlike in the Painted Bunting, we were
unable to directly evaluate if such ef fects were a result of age struc-
ture in wrens and cardinals, as it is difficult (or in the case of cardinals,
near im possib le due to molt str at eg y) to distinguish older and you ng er
birds from one another in most cases; but see our reasoning against
age as a factor in the discussion. For the full set of model comparisons
please see the supplementary materials (Tables S 2 – S 6 ).
FIGURE 3 Proportion of second- year (younger) male Painted
Buntings (relative to older males) inhabiting urban- edge and core
habitat s of San Antonio, Texas, USA , 2022.
FIGURE 4 Associations between light pollution and lateral eye size in (a) Carolina Wrens (Thryothorus ludovicianus) and (b) Northern
Cardinals (Cardinalis cardinalis), males and females pooled in each species, breeding across nine study sites in San Antonio, USA, 2022. Each
individual is represented with a single data point (faded dots) and colored shaded areas represent 95% confidence intervals.
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8
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JONES e t al.
4 | DISCUSSION
While recent research has documented behavioral responses of birds
to anthropogenic sources of light pollution (e.g., Dominoni et al., 2013;
Injaian et al., 2021), our findings provide some of the first evidence
that birds may respond to anthropogenic alterations of their sensory
environments through changes in eye morphology. Consistent with
our predictions, residential birds (i.e., Northern Cardinals and Carolina
Wrens) inhabiting core areas had smaller eyes than their edge coun-
terparts. Furthermore, we found a strong association between eye
size and the intensity of both light pollution and bright open areas in
both resi denti al sp eci es, suc h tha t bi rds in br igh te r, mor e li ght pol lut ed
areas had smaller eyes— suggesting an evolutionar y response of avian
eye size to sensor y environments altered by urbanization. This nega-
tive association also appears to coincide with decreasing variation in
eye size in more light polluted areas (Figure 4), which could reflect
directional selection toward smaller eyes in urban areas driving lower
genetic variation (e.g., Bar ton & Turelli, 1989; Walsh & Blows, 2009).
Future research is needed to examine the mechanism of observed
changes and other potential functional consequences for selection on
sm a lle r eye size . Imp ort ant ly an d in li ne wi t h our predi c t ion s , we fo und
no such relationships between eye size and light pollution in our two
migrator y species. Migrator y species may winter in more rural habi-
tats compared to their breeding grounds, and may use the stars and
other visual cues to navigate at night during migration (Moore, 1987 ).
Thus, migratory species may face conflicting selective pressures (via
variation in sensor y environments) on eyes size across different life
stages of their annual cycle. Consequently, future research is needed
to investigate potential differences in how residential and migratory
birds utilize their light environment (e.g., Ausprey et al., 2021) on
breeding versus wintering grounds.
Our findings on the effects of light pollution and brightness are
consistent with research demonstrating that smaller eyes are asso-
ciated with brighter environmental niches (Ausprey, 2021; Thomas
et al., 2004), and suggests that smaller eyes may be advantageous for
birds inhabiting the brighter, sensory polluted, urban habitats. Conse-
quently, species with smaller relative eye sizes (eye size controlled for
mass, used for interspecific comparisons; Ausprey, 2021) may be pre-
adapted to urban areas, and eye size may, in part, explain why some
species are extirpated from urban environments (i.e., why some spe-
cies become urban adaptors versus urban avoiders); larger- eyed spe-
cies inhabiting more contiguous, darker environments may not be able
to handle the brighter urban environments, as has been shown in trop-
ical landscapes (Ausprey et al., 2021; Martinez- Ortega et al., 2014).
Our findings are also in direc t contrast to predictions based on
other potential selective forces acting on eye size. For instance,
urban birds have exhibited shifts in their dawn chorus, singing earlier
in the morning in response to anthropogenic factors such as artificial
light at night and noise (Da Silva et al., 2 014; Ki & Cho, 2 014; Nordt
& Klenke, 2013; but see Marín-Gómez & Macgregor- Fors, 2021).
If light is the major factor driving shifts in dawn song, then larger,
light gathering eyes could allow birds to start their dawn chorus ear-
lier and reap additional reproductive benefits. However, while eye
size is associated with when birds begin their dawn chorus (Thomas
et al., 2002), there is also compelling research suggesting stronger
links between noise and dawn chorus than light (e.g., Arroyo- Solís
et al., 2013; Dorado- Correa et al., 2016). Consequently, factors such
as shifts in dawn chorus may not be a significant driver of eye size in
urban songbirds, as our findings suggest there is a stronger, oppos-
ing selec tive force of light acting upon eye size.
Additionally, unlike patterns of body size in male buntings, we
were unable to assess potential differences in eye size due to age
structure between edge and core environments due to difficulties
in ageing each residential species. Though we note an effect of
age is unlikely given that eye size, unlike body size, is not known to
and should not change as birds age (i.e., birds molt their wings and
tails each year, which can alter body size, whereas eye size should
not change), which would preclude differences between older and
younger birds. Eye size was also the only morphology where a dif-
ference was detected, whereas we would expect there to be corre-
sponding differences in the other morphologies if age was a factor.
Regardless, the association between eye size and urbanization raises
a number of important questions (e.g., How does the light micro-
environment [niches] differ in urban- core, urban- edge, and rural
birds? Do urban adaptors have a smaller relative eye size than urban
avoiders? How are potentially adaptive traits such as eye size main-
tained in urban habitat s, particularly at smaller spatial scales [is gene
flow ubiquitous among individuals]?) and demonstrates the need for
future research on this topic, particularly with regards to relation-
ships among eye size, ambient light microenvironment use, and dis-
assembly of avian communities as a result of urbanization (Senzaki
et al., 2020).
Contrary to our predictions, we found no effect of urbaniza-
tion on the body siz e of reside nt ia l son gb irds, wit h m as s and frame
size being similar in edge and core environments in both species.
These findings are therefore in direct contrast to past hypotheses
predicting changes in body size of urban birds, including the pre-
dicted effects of urban heat islands (Bergman's rule; Salewski &
Watt, 2017 ), urban food resources (resource rule; McNab, 2010),
and habitat fragmentation (island rule; Clegg & Owens, 2002).
However, these findings are in line with our comparisons of en-
vironmental characteristics among sites, which suggests there
were no significant differences in snapshot noise pollution or
mean annual temperatures between urban- edge and urban- core
areas that may preclude selection for smaller body size. Addition-
ally, we did not direc tly test parameters associated with some of
these hypotheses (e.g., variation in food resources, degree of hab-
itat fragmentation), thus selective pressures that are associated
with such parameters could have additive effects such that we
detected no changes in body size among edge and core individ-
uals. Regardless, our findings are consistent with recent studies
documenting similar body sizes in urban and more natural areas in
other songbirds (e.g., Evans, Gaston, Sharp, McGowan, & Hatch-
well, 2009; Giraudeau et al., 2015; Kozlovsky et al., 2021), but
contradict findings in the House Sparrow (Passer domesticus) and a
few other species (e.g., Caizergues et al., 2018; Liker et al., 2008;
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9
JONES et al.
Meillere et al., 2015). Thus, these findings also contribute to and
are consistent with general conclusions drawn from the past lit-
erature, in which neutral and negative results suggest there is no
cle ar lin k be twee n body size an d urban– rural habitats (re viewe d in
Sepp et al., 2017). Ultimately, such findings suggest that changes
(or lack thereof ) in avian body size in response to urbanization may
be species, site, and context specific (e.g., Evans, Gaston, Sharp,
McGowan, & Hatchwell, 2009; Strubbe et al., 2020), rather than
being governed by overarching, selective forces known to medi-
ate morphological differences at larger geographic and taxonomic
scales.
While we found no differences in body size among residential
songbirds, our findings on the migratory Painted Bunting provide
an important example of context specific effects of urbanization
on body size. Buntings inhabiting core areas had smaller frame
sizes than their edge counterparts, which at first glance could be
considered evidence of phenotypic divergence between urban edge
and core populations. However, our post- hoc analyses suggest that
differences were a result of variation in proportions of SY buntings
inhabiting edge and core habitats (Figure 4), with there being more
SY buntings in core areas and SY buntings being, on average, smaller
than ASY buntings. Thus, differences in body size between edge and
core areas is likely the indirect effec t of urbanization on the demo-
graphics and settlement patterns of buntings. Our study highlights
a potential mechanism for such patterns, as we found a negative
association between bunting body size (both mass and frame size,
serving as proxies) and noise pollution across edge and core habitats.
This suggests urban noise may act as a stressor, creating novel hab-
itats that deter older birds and makes it more likely for SY buntings
to colonize core habitats, as younger animals are of ten more explor-
atory and less neophobic compared to older individuals (e.g., Berg-
man & Kitchen, 2009; Biondi et al., 2010; Lamberty & Gower, 1992).
Additionally, differences in the proportion of younger birds between
habitat s may reflect their quality, as older, higher qualit y individuals
often arrive to breeding grounds earlier and occupy higher quality
territories (e.g., Lozano et al., 1996; Smith & Moore, 2005; Stewart
et al., 2002), which could relegate younger birds to the remaining,
noisier, poorer quality core environments. Lastly, differences in age-
specific survival bet ween edge and core areas could coincide with
demographic differences in those populations (e.g., Ibanez- Alamo
et al., 2018; Salmon et al., 2016), with core areas acting as a sink for
the species. Furthermore, if most of these SY buntings fledged from
nests in non- core areas, that may help explain, in part, the lack of eye
divergence between edge and core areas. To date, however, results
on urban drivers of age structure remain equivocal (Evans, Gaston,
Sharp, McGown, Simeoni, et al., 2009; Kozlovsky et al., 2021), high-
lighting the need for future studies on interactions between urban-
ization, age structure, and phenotypic change.
Our findings on the age structure of Painted Buntings highlight
an important consideration for future studies examining associations
between urbanization and variation in phenotypic traits. Indeed,
without accounting for differences in age and age structures, we
may have erroneously concluded that our results provide evidence of
phenotypic divergence between edge and core populations resulting
from an evolutionary response to urbanization. Differences in age
structure between urban and more natural habitats remains a largely
overlooked factor that can mediate associations between urbaniza-
tion and phenotypic traits of interest (Kozlovsk y et al., 2021). While
some studies have documented clear differences in phenotypic traits
between urban and rural habitat s (e.g., Liker et al., 2008; Meillere
et al., 2015; Smith et al., 2021), few studies have explicitly tested for
the confounding effect s of age on avian responses to urbanization.
And as our findings with the buntings clearly demonstrate, failure to
explicitly test for relationships between urbanization, age, and age
str uctures makes it dif ficult to fully address potentia l dri ver s of ph e-
notypic variation in the face of urbanization (Kozlovsky et al., 2021),
and as a consequence, may produce misleading result s.
In summary, we found evidence that light levels, both day-
time brightness occurring through urban development and arti-
ficial light at night (light pollution), may select for smaller eyes in
resident bird species inhabiting urban core areas as compared to
urban edges. Though the underlying mechanisms of this relation-
ship remain unclear, being a year- round resident of light polluted
areas appears key to this phenotypical pattern. Our findings also
suggest that migratory birds returning to urban areas vary in their
territory selection based on age and experience rather than sen-
sory pollution per se, such that younger birds appear relegated to
territories with higher noise levels. Future work should explore
the me ch an isms dri ving variation in son gb ir d ey e si ze acr os s urban
and more natural environments (i.e., direct exposure of light at the
nest during growth, survival, foraging, and breeding ef ficiency
under different light environments, physiological pathways via
mother and nestlings, and dispersal patterns), microhabitat use
of sensory polluted environments across different avian life his-
tory stages, and consequences of selection on songbird eye size
in urban areas.
ACKNOWLEDGMENTS
This research was funded with support from the Life Sciences De-
partment at Texas A&M University- San Antonio, the College of Arts
and Sciences, Friends of Government Canyon, and Texas Eco- Lab.
This work would not be possible without the dedicated efforts of
Kristi Bradley, Theresa Edwards, Victoria Garcia, Destiny Gonzales,
Christina Helmick, Sierra Rodriguez, Katarina Scalercio, and Ryan
Thornton. We are grateful to Texas Parks and Wildlife, Govern-
ment Canyon State Natural Area, San Antonio Parks and Recreation,
Mitchell Lake Audubon Center, and the San Antonio River Authority
for access to study sites.
CONFLICT OF INTEREST STATEMENT
The authors have no conflicts of interest or competing interests.
DATA AVAIL AB I LI T Y STATE MEN T
The data that support the findings of this study are openly available
in the Illinois Databank at https://doi.org/10.13012/ B2IDB - 60108
27_V1 .
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10
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JONES e t al.
ORCID
Todd M. Jones https://orcid.org/0000-0002-1658-6531
Jennifer N. Phillips https://orcid.org/0000-0002-0014-2995
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J. N. (2023). Phenotypic signatures of urbanization? Resident,
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