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Received: 26 October 2017 Revised: 14 February 2018 Accepted: 2 March 2018 DOI: 10.1002/ece3.4038
ORIGINAL RESEARCH
Bill size variation in northern cardinals associated with anthropogenic drivers across North America Colleen R. Miller
| Christopher E. Latimer | Benjamin Zuckerberg
Department of Forest and Wildlife Ecology, University of Wisconsin-Madison, Madison, WI, USA Correspondence Colleen R. Miller, Department of Forest and Wildlife Ecology, University of WisconsinMadison, Madison, WI, USA. Email:
[email protected]
Abstract Allen’s rule predicts that homeotherms inhabiting cooler climates will have smaller appendages, while those inhabiting warmer climates will have larger appendages relative to body size. Birds’ bills tend to be larger at lower latitudes, but few studies have tested whether modern climate change and urbanization affect bill size. Our study explored whether bill size in a wide-ranging bird would be larger in warmer, drier regions and increase with rising temperatures. Furthermore, we predicted that bill size would be larger in densely populated areas, due to urban heat island effects and the higher concentration of supplementary foods. Using measurements from 605 museum specimens, we explored the effects of climate and housing density on northern cardinal bill size over an 85-year period across the Linnaean subspecies’ range. We quantified the geographic relationships between bill surface area, housing density, and minimum temperature using linear mixed effect models and geographically weighted regression. We then tested whether bill surface area changed due to housing density and temperature in three subregions (Chicago, IL., Washington, D.C., and Ithaca, NY). Across North America, cardinals occupying drier regions had larger bills, a pattern strongest in males. This relationship was mediated by temperature such that birds in warm, dry areas had larger bills than those in cool, dry areas. Over time, female cardinals’ bill size increased with warming temperatures in Washington, D.C., and Ithaca. Bill size was smaller in developed areas of Chicago, but larger in Washington, D.C., while there was no pattern in Ithaca, NY. We found that climate and urbanization were strongly associated with bill size for a wide-ranging bird. These biogeographic relationships were characterized by sex-specific differences, varying relationships with housing density, and geographic variability. It is likely that anthropogenic pressures will continue to influence species, potentially promoting microevolutionary changes over space and time. KEYWORDS
Allen’s rule, bill size, climate change, housing density, microevolution, morphology
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2018;1–11.
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1 | I NTRO D U C TI O N
Tattersall et al., 2009; Van de Ven et al., 2016) or heat conservers in colder climates (Danner & Greenberg, 2015; Hagan & Heath, 1980).
For over 150 years, biogeographers have codified their obser-
In recent years, there has been a renewed interest in Allen’s rule
vations of the natural world in a set of rules explaining variabil-
due to the microevolutionary implications of modern climate change.
ity in species’ traits. Biogeographic principles such as Gloger’s
Modern climate change has resulted in unprecedented shifts in tem-
rule (Gloger, 1833), Allen’s rule (Allen, 1877), Bergmann’s rule
perature and precipitation throughout the globe (IPCC Report 2014).
(Blackburn, Gaston, & Loder, 1999; Gardner, Peters, Kearney,
In North America, climate change has and will continue to impact cli-
Joseph, & Heinsohn, 2011; Scholander, 1954), and Rapoport’s rule
mate patterns, as global temperatures have increased approximately
(Rapoport, 1982) documented broad latitudinal differences in ani-
1.5°C over the past 100 years (Melillo, Richmond, & Yohe, 2014). As
mal pigmentation, appendage size, body size, and range character-
a result, whether changes in global climate could promote changes in
istics. These principles describe not only the geographic variation
species’ traits remains a question (Gienapp, Teplitsky, Alho, Mills, &
in traits among species, but also variation across species’ popula-
Merilä, 2008). While many studies have focused on Allen’s rule over
tions, and serve as a lasting framework for exploring trait diversity
space (Danner & Greenberg, 2015; Friedman et al., 2017; Greenberg
across the world.
& Danner, 2012; Greenberg, Danner et al., 2012; Greenberg,
Given the latitudinal nature of many biogeographic princi-
Cadena et al., 2012; Symonds & Tattersall, 2010), few have evalu-
ples, climate is considered the most likely mechanism underlying
ated changes in bill size over time (Campbell-Tennant et al., 2015).
variability in species’ traits. For example, Allen’s rule predicts that
In one study on Australian parrots, the authors found evidence that
homeotherms with relatively smaller appendages (high volume-to-
bill sizes increased over time, putatively as an adaptation to ther-
surface ratio) can minimize heat loss and persist in colder climates,
mal stress of rising maximum temperatures (Campbell-Tennant et al.,
while species with larger appendages (low volume-to-surface ratio)
2015). Many other studies have focused on climate-induced changes
have more efficient heat dissipation in warmer environments (Allen,
over time in traits such as plumage coloration (Evans & Gustafsson,
1877). Although the mechanism of thermal adaptation as a driver of
2017; Karell, Ahola, Karstinen, Valkama, & Brommer, 2011), but not
appendage size variation has received mixed empirical support (Alho
in bill size. Together, these studies suggest that birds can respond to
et al., 2011; Nudds & Oswald, 2007), Allen’s rule is often invoked
changes in climate with potential implications for morphological and
as a possible explanation for geographic variation in bill size for
microevolutionary change.
birds (Danner, Greenberg, & Sillett, 2014; Friedman, Harmáčková,
Much of the environment which species inhabit is currently ex-
Economo, & Remeš, 2017; Greenberg & Danner, 2012). Avian bills
hibiting rapid environmental change both in climate and in land use
play an important function in thermoregulation due to vascularized
change. Modern climate change is occurring over a rapidly shift-
tissue mediating heat transfer and mitigating water loss (Danner
ing landscape, and many regions have experienced widespread
et al., 2017; Tattersall, Andrade, & Abe, 2009; Tattersall, Arnaout,
changes in urbanization (Arnfeld, 2003; McKinney, 2006). Several
& Symonds, 2016), and bill size tends to correlate with climatic gra-
bird species are considered synanthropes that rely on bird feeders
dients both within and across species (Symonds & Tattersall, 2010).
as a source of supplemental food and, in some cases, can survive
For example, populations of saltmarsh sparrows (Ammodramus
and thrive in urban areas (Bosse et al., 2017; Marzluff, 2014). For
caudacutus) (Greenberg, Danner, Olsen, & Luther, 2012) and song
example, northern cardinals reach higher abundances in urban
sparrows (Melospiza melodia) (Danner & Greenberg, 2015) inhabiting
areas than in rural areas due to warmer winter temperatures
warmer regions have larger bills compared to populations in colder
and supplemental food resources (Leston & Rodewald, 2006).
regions.
Seminal studies documenting a relationship between seed size and
The relationship between bill size and climate is complicated,
Galapagos finches’ bill size demonstrated the importance of re-
and differences in aridity and minimum or maximum temperature
source availability on bird morphology as seasons associated with
can modify the role of bills in thermal adaptation. Patterns in the
large, tough seeds selected for birds with larger bills, while sea-
relationship between bill size and temperature often interact with
sons with smaller seeds selected for smaller bills (Boag & Grant,
aridity: The positive relationship between bill size and temperature
1981, 1984). With the onset of bird feeding as a popular pastime
is amplified in more arid environments (Campbell-Tennant, Gardner,
in many urban areas, supplemental seed may influence bill mor-
Kearney, & Symonds, 2015; Greenberg & Danner, 2012). This could
phology (Robb, McDonald, Chamberlain, & Bearhop, 2008). For
be because birds lack sweat glands and the passive dissipation of
example, a study conducted on house finches (Carpodacus mexi-
dry heat by bills could substantially reduce the amount of respira-
canus) in the Sonoran Desert found that birds living in urban areas
tory water lost by active means such as gular flutter and panting
had larger bills with larger bite forces, likely a product of habitat-
(Greenberg, Cadena, Danner, & Tattersall, 2012; Van de Ven, Martin,
specific selection pressures (Badyaev, Young, Oh, & Addison,
Vink, McKechnie, & Cunningham, 2016). In more temperate environ-
2008). Genomic regions under differential selection contain can-
ments, minimum and maximum temperatures can influence morphol-
didate genes for bill morphology across populations of great tits
ogy through their effects on thermal metabolism (Campbell-Tennant
(Parus major), with birds in the United Kingdom evolving longer
et al., 2015; Fristoe et al., 2015; Root, 1988b), and bills can function
bills in response to supplementary feeding (Bosse et al., 2017).
as either heat dissipaters in hot climates (Symonds & Tattersall, 2010;
Given the increasing prevalence of urban areas (McKinney, 2006),
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MILLER et al.
it is likely that the characteristics of urban areas (e.g., urban heat islands, supplemental food) may complicate the predictions of biogeographic principles such as Allen’s rule (Faurby & Araújo, 2016). The goal of our study was to explore spatiotemporal changes in the bill size of northern cardinals (Cardinalis cardinalis cardinalis), a wide-r anging, non-migratory, synanthropic species that has been expanding its range northward over the past century (Dow & Scott, 1970; Halkin & Linville, 1999). The northward range expansion of cardinals has been associated with increases in winter minimum temperatures that may relax thermoregulatory constraints for populations occurring in northerly latitudes (La Sorte & Thompson, 2007; Root, 1988a; Zuckerberg, Woods, & Porter, 2009; Zuckerberg et al., 2011) and shifting resources due to the rise in popularity of bird feeders in northerly areas (Morneau et al., 1999). To test the predictions of Allen’s rule, we measured bills from northern cardinal museum specimens collected across
F I G U R E 1 Map of collection locations of the 605 northern cardinal specimens used in this study indicated by gray circles. Black boxes represent the three locations at which temporal analyses were conducted: Chicago, Illinois (a); Washington, D.C. (b); and Ithaca, New York (c)
North America. We hypothesized that cardinal bill sizes would (1) be larger in warmer and more arid climates, (2) increase in regions
each specimen three times and used the average of those mea-
characterized by warming temperatures, (3) be larger in more
surements to quantify bill surface area. To avoid observer bias,
urban areas, and (4) increase in areas characterized by increasing
a single observer (C.R.M.) measured all specimens. We measured
housing density. By testing these predictions across a continental
tarsus length of each specimen as a proxy for body size in our
scale, we provide a novel examination of Allen’s rule during a pe-
analyses (Andrew, Awasthy, Griffith, Nakagawa, & Griffith, 2017;
riod of rapid environmental change.
Danner et al., 2014; Labocha & Hayes, 2012; Teplitsky, Mills, Alho, Yarral, & Merilä, 2008). Bill measurements relative to the
2 | M ATE R I A L S A N D M E TH O DS 2.1 | Specimen measurement
nares and skeletal measurements are considered robust in museum specimens; therefore, we assumed that our bill measurements from museum specimens reflected the measurements of a live specimen (Field, Lynner, Brown, & Darroch, 2013; Wilson
To quantify bill size of northern cardinals throughout their range,
& McCracken, 2008). Although tarsus length has been shown to
we took measurements of 605 museum specimens (Figure 1; Table
vary according to Allen’s rule in other species (Nudds & Oswald,
S1). We used adult specimens that were collected in the wild and
2007; Symonds & Tattersall, 2010), we considered tarsus length
included information on collection locality and date. We took all
an appropriate proxy of passerine body size that has been used
measurements using Fowler digital calipers with 0.02 mm precision
in previous studies and which positively correlates with skeletal
(Fowler Xtra-Value Cal Electronic Calipers Model No. 54-101-150-2).
body size (Senar & Pascual, 1997; Jawor et al. 2004; Bosse et al.,
Only specimens of the Linnaean subspecies Cardinalis cardinalis
2017; Danner et al., 2017; Andrew et al., 2017).
cardinalis were included in this analysis. This subspecies occupies a broad range across eastern North America, which has expanded northward over time, while retaining stable genetic diversity (Smith
2.2 | Climate and housing density data We obtained climate data collected in the United States between
et al., 2011). We assumed a circular elliptical cone could approximate the
1924 and 2016 using the R package “RFc” (Grechka et al., 2016).
shape of the bill and estimated bill surface area using the formula for
We extracted our climate data from the CRU CL 2.0, CESM1-BGC
the lateral surface area of a cone:
CMIP5 rcp85, and WorldClim 1.4 current datasets (Arora et al.,
(
W+D 4
)
2013; Hijmans, Cameron, Parra, Jones, & Jarvis, 2005; New, Lister, ×L×π
where L is the bill length measured from the proximal side of the
Hulme, & Makin, 2002). Climate variables represent monthly averages at each location. All climatic variables were z-standardized to allow for easier interpretation of the coefficient estimates.
nares to the bill tip; W is the bill width measured at the proximal
We calculated average air maximum and minimum temperature
side of the nares; and D is the depth of the bill measured at the
and relative humidity data for 30 years prior to collection at each
point of the proximal side of the nares (Danner & Greenberg,
location. These data represented the climate normal of a given geo-
2015). Here, we use the term “proximal” in reference to the center
graphical area. We also calculated climate variables for 4 years prior
of mass, where the proximal side of the bill is the side closest to
to specimen collection date at each location to represent the ap-
the head and torso. We avoided dependence on facial plumage
proximate generation time of northern cardinals. This approximate
presence using the nares as a measurement guide. We measured
s generation time was derived from a + 1−s , where a is age at normal
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MILLER et al.
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breeding maturity for females and s is survival rate (Saether et al.,
For purposes of visualization, we used geographically weighted
2005). Age at maturation for females was 1 year (Halkin & Linville,
regression (GWR) to allow modeled relationships between climate
1999; Richmond, 1978). We used an adult survival rate estimated by
and bill surface area to vary across geographic regions (Charlton &
the Monitoring Avian Productivity and Survivorship (MAPS) program
Fotheringham, 2009). GWR is primarily an exploratory approach,
using transient Cormack–Jolly–Seber models (Desante, Kaschube, &
which allows local and regional non-stationarity in parameter co-
Saracco, 2015; MAPS 2016).
efficients. We included two separate relationships in this analysis,
We used housing density data for the United States between
investigating the relationship between bill surface area and relative
1940 and 2016 obtained from US census data aggregated at the par-
humidity, and bill surface area and relative humidity x average mini-
tial block level (Hammer, Stewart, Winkler, Radeloff, & Voss, 2004).
mum temperature for all birds. We used fixed bandwidths (selected
Partial blocks are mapping units intermediate in scale between census
using AIC c in R package “spgwr”) to inform spatial weighting of each
block groups and block groups. As these data are a product of the US
data point (Bivand & Yu, 2008) and estimated local coefficients using
census, they provide decadal estimates of housing density. Therefore,
a Gaussian kernel function in the R package “spgwr” (Bivand & Yu,
we created 30-year normal of housing density to match the climate
2008).
data. Housing density served as a proxy both for the urban heat island
Due to a sparsity of samples during the full 85-year period over
microclimate and for the presence of supplemental seed. We used
all regions within our study range, we investigated temporal variation
mean housing density estimated at a given specimen’s coordinate.
of bill surface area in three separate subregions that had adequate coverage across the 85-year time span: Chicago, IL, Ithaca, NY, and
2.3 | Analysis
Washington, D.C. (Figure 1). The northern cardinal dispersal distance is conservatively estimated at 10 km; therefore, we used a 10 km ra-
As bill surface area often co-varies with body size in birds (Field et al.,
dius distance for each location in this subregion analysis (Ausprey
2013), we took the residuals of bill size regressed on tarsus length as
& Rodewald, 2013; Donovan & Flather, 2002). Using general linear
a measure of corrected bill size. Given concerns about the use of
models, we tested the relationship between bill surface area and
residuals (Freckleton, 2002), we also included tarsus as a predictor in
year, bill surface area and housing density, and bill surface area and
all models (Tables S2 and S3). Positive residuals indicate a larger bill
minimum temperature for three groups: females, males, and all birds.
size relative to body size, while negative residuals indicate bill size
We used decadal estimates for housing density in this temporal anal-
proportionately smaller than body size. Northern cardinals express
ysis. R 2 values for our generalized mixed models and simple linear
sexual dimorphism not only in body size, but also in corrected bill
models were calculated using the package “MuMIn” in R (Barton,
surface area. Males have larger bills than females throughout their
2018). We z-standardized all independent variables to allow straight-
range (Figure S1) and may experience higher exposure to air tem-
forward comparison and interpretation of the coefficient estimates
perature and humidity variation as a result of singing more compared
and conducted all analyses in R Version 3.3.1 (R Core Team 2016).
to females (Conner, Anderson, & Dickson, 1986) and increased respiratory water loss (Greenberg & Danner, 2012; Greenberg, Cadena et al., 2012). Therefore, we investigated the sexes separately for all analyses. We used linear mixed models (LMM) using a Gaussian error dis-
3 | R E S U LT S 3.1 | Geographic differences in bill size
tribution to assess the variation in bill surface area across range-
While we conducted analyses for both average minimum and maxi-
wide gradients of temperature and relative humidity for all birds and
mum temperatures (Table S4), we present results for minimum tem-
each sex separately. We ran two sets of models: one set for average
perature because minimum temperature and maximum temperature
minimum temperature and one set for average maximum tempera-
values were highly correlated (r = .96). We selected minimum tem-
ture. We first aggregated our raw data by sex and collection loca-
perature because the cardinal range has shifted north over the past
tion. We weighted cardinal bill surface area by the number of birds
century (Halkin & Linville, 1999; La Sorte & Thompson, 2007) and is
measured at each location to account for differences in the precision
thought to be related to warming minimum temperatures. We hypoth-
of estimates at each location and included an exponential correla-
esized that minimum temperatures would play a larger role in cardinal
tion structure based on geographic coordinates accommodating
ecology as their northerly range boundary, and hence expansion, is
spatial model inference (N = 345). We included the fixed effects
correlated with isotherms of minimum temperature (Root, 1988b).
of year, temperature, housing density, and humidity. Temperature,
Cardinals had smaller bills in more arid regions (β = −8.66, SE = 1.91,
housing density, and humidity were all taken relative to their 30-
p = .00), with most of this pattern being exhibited by male as opposed
year average. We also included an interaction between temperature
to female birds (Table 1). This relationship was modified by average
and humidity and an interaction between temperature and housing
minimum temperature, with birds residing in warmer areas having a
density. We incorporated observation ID as a random effect to serve
weaker relationship with relative humidity than cardinals residing in
as a grouping factor for the spatial correlation matrix. We ran mod-
cooler areas (β = 4.08, SE = 1.92, p = .03) (Figure 2). Contrary to our
els using the R package “nlme” (Pinheiro, Bates, DebRoy, & Sarkar,
predictions, cardinals found in areas with higher housing density had
2011). We used an alpha level of 0.05 for significant results.
smaller bill surface areas (β = −3.62, SE = 1.44, p = .01). We found no
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TA B L E 1 Results of the model of bill surface area across the United States for female and male northern cardinals Variable
Estimate
Standard error
p-value
15.644
4.183
