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Mar 2, 2018 - housing density and temperature in three subregions (Chicago, IL., .... specific selection pressures (Badyaev, Young, Oh, & Addison,. 2008).
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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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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.

4      

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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MILLER et al.

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