Passerine and Near Passerine Diversity, Richness, and Community Responses to A

Passerine and Near Passerine Diversity, Richness, and Community Responses to a

Rural to Urban Gradient in Southeastern Ohio

______

A thesis presented to

the College of Arts and Sciences

Ohio University

______

In Partial Fulfillment

of the Requirements for Graduation

from the College of Arts and Sciences

with the degree of

Bachelor of Science in Biological Sciences- Wildlife Biology

______

By

Jessica E. Howell

May 2014

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This thesis has been approved by

The College of Arts and Sciences and the Department of Biological Sciences

Dr. Donald Miles

Professor, Biological Sciences

Thesis Advisor

Dr. Janet Duerr

Professor, Biological Sciences

Departmental Honors Coordinator

Dr. Robert Frank

Dean, College of Arts and Sciences

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Abstract:

Over 50% of the world’s human population lives in cities and the number is steadily rising. Urbanization involves a unique set of environmental characteristics including greater imperviousness of surfaces, higher temperatures, and higher noise and light levels than natural systems. Urban development favors resident species of birds, granivores and omnivores, and rock and cavity nesters over migrants, insectivores, and ground nesters. This leads to differences in colonization success among species. In this study I assessed species richness, diversity, abundance, and guild composition of passerine and near passerine birds in an urban area situated in a rural landscape. I hypothesized that diversity should be lowest in the most urbanized areas and highest in the rural areas, abundances of species should differ among habitats on the rural to urban gradient, and avian communities of urban and rural areas should be unique. The most rural site had the highest species richness and the urban area had the lowest. Species diversity was greater in more rural areas. The abundance of invasive species increased and migrant species richness decreased towards the urban core, and feeding and nesting guild structures differed. These results have wildlife management, biodiversity, and social implications at the local as well as global level.

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Acknowledgements:

There are so many people who have helped me along this journey. First, thank you to my advisor Dr. Don Miles for sparking my interest in Ornithology and giving me the opportunity to work in the field through this project. Second, thank you to Dr.

Kelly Williams-Sieg for serving as a second advisor and patiently helping me with statistics and being a source of encouragement along the way. Third, to my loving family: my mother April Howell, father Dana Howell, sister Meghan Howell, aunt

Shirley-Ann Miller, aunt Ronda Ghosh, uncle Sam Ghosh, and cousin Rani Ghosh for always encouraging me to follow my dreams of being a wildlife biologist and conservationist, and for all their support over the good and bad times over the past four years of my undergraduate college career. I cannot thank them enough for all their love and guidance. Included in my family are also my dogs and cats, especially my dog Phoebe Patriot Howell, for helping to instill a love of nature in me and inspiring me to protect wildlife. Fourth, to my friends for making me smile and helping me keep my sanity, in particular Pradeep Cheriyan, Aspen Cutlip, Amelia

Adams, Mumtaz and Reda Gardezi, and Jordan and Samantha Fitch. Finally, to the staff of the Ohio University Department of Biological Sciences, for teaching me so much and giving me a sense of belonging over the past four years. There are so many people that have touched my life in some way and that have helped me grow as a student. I feel extremely blessed for all the amazing people in my life, and I could not have done this without them. 4

Table of Contents

Introduction ...... 6

The Urban Environment ...... 6

The Ecology of an Urban Avifauna ...... 9

Avian Population Dynamics...... 9

Avian Responses to Urbanization ...... 16

Urban Exploiters...... 16

Urban Adaptors...... 18

Urban Avoiders...... 19

General Trends...... 21

Previous Research and Predictions ...... 21

Current Project ...... 22

Project Goals...... 23

Project significance...... 24

Methods ...... 26

Data Collection ...... 26

Data Analysis ...... 27

Results ...... 30

Species Richness, Abundance, Diversity, and Evenness ...... 30

Predator Presence ...... 32

Species Accumulation Curves and Number of Unobserved Species ...... 32

Species Differences by Site Nonmetric Multidimensional Scaling ...... 33 5

Guild Univariate Model ...... 33

Discussion ...... 34

Literature Cited ...... 41

Figures Legend ...... 50

Figures ...... 52

Tables ...... 61

Appendices ...... 67

Appendix A: Photographs of Study Sites ...... 67

Appendix B: Google Maps/ACME Planimeter Satellite Images of Study Sites ...... 70

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Introduction The Urban Environment

Increasing human population and activities have been progressively altering landscapes and ecosystems on a global scale. Estimates of the amount of land converted in some way by humans are as high as one third of global land surface

(Vitousek et al., 1997). The most drastic of these changes occurs with urbanization; which carries a unique set of characteristics from ground surface to air composition.

The global population of over 7 billion people and growing (United States Census

Bureau, 2014) is becoming increasingly concentrated in cities. While in 1990 only

10% of the global population lived in cities, today it is over 50% and this is increasing as well, with over 95% of net population increase for the next 50 years expected to be in cities (Grimm et al., 2008). This population and city growth involves enormous amounts of resources and copious amounts of waste; representing 60% of residential water use and almost 80% of global carbon emissions (Grimm et al., 2008).

Urbanization is defined as high human abundance compacted into residential and industrial areas, along with its associated effects; and an urban center is identified by having over 2500 people (Chace & Walsh, 2006). A change in thinking has taken place in recent years regarding urbanization and landscape ecology. For much of the

20th century, cities were viewed as human-induced destruction of ecosystems not within the scope of ecology (Grimm et al., 2008). Since its inception in the 1970’s, urban ecology is a growing discipline in which cities are considered unique ecosystems (Clergeau et al., 1998). Whereas earlier research approached the city as an experimental treatment with rural areas as a control, current approaches examine rural 7

to urban areas as an ecological gradient (Gering & Blair, 1999). It is now understood that the urban landscape represents a unique combination of functions, disturbances, structures, and stresses (Pickett et al., 1997).

Urbanizing areas show a gradient of increasing human population, road density, soil compression and alkalinity, soil and air pollution, average air temperature, average precipitation, and percent impervious surface among other variables

(McKinney, 2002). The general pattern of urban centers is highly concentrated built structures and people in a core surrounded by intermediate suburban areas (Decker et al., 2000). Cities have their own set of inputs and outputs, resulting in substantial alteration of biogeochemical cycles. Water supply is manipulated and the high percentage of impervious surface (i.e. concrete) causes increases in runoff, decreases in percolation to groundwater, and a more rapid flow of nutrients downstream (Kaye et al., 2007). Carbon dioxide increases by over 100 ppm going from rural to urban areas (Kaye et al., 2007). Nitrogen, aerosols, metals, and ozone are also at higher atmospheric concentrations in cities (Kaye et al., 2007). Impervious surfaces absorb light energy during the day and release this as heat during the night, contributing to a phenomenon known as the Urban Heat Island (Kaye et al., 2007). This leads to short and long term temporal effects of higher average and minimum daily temperatures, longer seasonal warm periods, and more frost-free days (Kaye et al., 2007). Point sources of pollution in water, air, and soil lead to larger regional concerns such as eutrophication and smog (Grimm et al., 2008). 8

A functional consequence of urbanization is the change in abiotic and biotic characteristics of habitats that may support wild populations. These changes involve microhabitat (temperature, light, exposure, noise, etc.), vegetation, decomposition rates, and nutrient cycling (Hansen & Urban, 1992). Increased levels of nitrogen and carbon dioxide as well as increased temperature affect plant physiology and microbial growth (Faeth et al., 2005; Kaye et al., 2006). Increased primary productivity, partially resulting from the urban heat island effect, may reduce competition at all trophic levels (Faeth et al., 2005). Furthermore, heterogeneity in urban flora due to different landscape design (habitat replacement) by humans results in more variation in trophic dynamics in urban areas (Faeth et al., 2005).

Ecologists recognize four categories of habitat replacement: built habitat

(human made structures), managed vegetation (green spaces that are maintained), ruderal vegetation (spaces that have been cleared but are abandoned and undergoing succession), and remnant native vegetation (isolated fragments of original vegetation)

(McKinney, 2002). These different patches not only have higher heat and pollutants as previously discussed, but increased light and noise levels from buildings, industrial activities, and automobiles (Chamberlain et al., 2009). Artificial night light drastically alters habitat, potentially disorienting fauna (Nordt & Klenke, 2013). Urban noise is of higher amplitude and lower frequency than natural background noise, with a diurnal periodicity (Nordt & Klenke, 2013). The associated primary productivity increase and extended warm seasons create a bottom-up trophic cascade that leads to increased arthropod abundances (Faeth et al., 2005). Higher trophic levels and vertebrate 9

abundances depend on the ability of individuals to synurbanize- colonize and adapt to urban conditions (Luniak, 2004).

The Ecology of an Urban Avifauna

Birds serve as important indicators of the effects of urbanization because they are sensitive to habitat and community structure changes. Moreover because birds are widespread, conspicuous, and highly diversified in ecology and taxonomy (Savard,

Clergeau, & Mennechez, 2000; Palamino & Carrascal, 2006), changes in species composition and abundance are more noticeable. Current estimates place global avian diversity at over 10,000 described species (Lepage, 2014). Species in the order

Passeriformes compromise over 50% of the total species, and dominate urban avian communities (Chamberlain et al., 2009).

Urban centers encompass a variety of novel ecological niches, which creates an “ecological vacuum”, an attractant to individuals and populations (Luniak, 2004).

However, due to the drastic changes from natural systems, successful city-dwelling individuals must exhibit a great degree of ecological, demographic, and behavioral plasticity, especially in habitat and diet (Luniak, 2004).

Avian Population Dynamics.

Population Density.

Urban center avian populations are typically at higher densities, with smaller territories per individual (Luniak, 2004). Four factors can lead to higher densities: greater offspring production, higher survival rates, more returns to the same site, and greater attractiveness of sites (Stracey & Robinson, 2012). The attraction and 10

accumulation of birds in urban centers is most likely mainly because of higher food densities (Shochat, Lerman, & Fernandez-Juricic, 2010) and milder winter microclimates (Leston & Rodewald, 2006), but also because of space limitation and lower mortality by a paucity of avian predators (Luniak, 2004). The urban environment offers many anthropogenic trophic subsidies: bird feeders, garbage, and exotic vegetation (Shochat, Lerman, & Fernandez-Juricic, 2010). Rodewald and

Shustack (2008) found a 2.6 times higher food abundance in urban environments compared to rural habitats. Warmer winter temperatures reduce the cost of maintaining high body temperatures, which lowers food requirements and mortality

(Leston & Rodewald, 2006).

Predation.

Although results are somewhat conflicting, many studies have shown that predation rates decrease from rural habitats to urban areas (Gering & Blair, 1999;

Luniak, 2004). Stracey (2011) found that urban predation rates were similar to rural habitats, and this held across years. The most well-studied predators are raptors and domestic cats (Felis catus). Generalist predators such as jays and crows (family

Corvidae) are more common than raptor species that are often more specialized predators (Sorace & Gustin, 2009). However, several raptor species including

American Kestrel (Falco sparverius), Peregrine Falcon (Falco peregrinus), Cooper’s

Hawk (Accipiter cooperii), Red-Tailed Hawk (B. jamaicensis) and Red-Shouldered

Hawk (B. lineatus) have been commonly found in cities (Chace & Walsh, 2004). Free ranging domestic cats in urban centers showed similar depredation rates to rural areas 11

despite higher densities (Lepcyzk, Mertig, & Liu, 2003). However it is important to note that on a national scale free-ranging and feral cats constitute the largest anthropogenic source of avian mortality, killing millions of birds each year (Loss et al., 2014).

Parasitism and Disease.

Parasitism is another factor affecting bird density. Parasites have an impact on disease prevalence and strength as well as host susceptibility to other factors influencing survival and fitness; parasites may play a major role in determining what species and individuals can succeed in urban centers (French, 2012). Birds are hosts to a variety of macro and micro parasites (French, 2012).

Theory predicts a positive relationship between host density and parasite prevalence; so urban centers would be expected to have higher parasite loads due to increased contact and transmission as well as higher stress and poor quality habitat

(French, 2012). Bradley et al. (2008) found that West Nile Virus prevalence increased on a gradient from rural to urban areas and Boal et al. (1998) found that Trichomonas was increased in urban hawks in Tucson, Arizona. However Geue and Partecke

(2008) found lower blood parasite levels in urban blackbirds in Munich, Germany.

These results may indicate inherent parasite and host differences and/or other factors; more research is needed in this area (French, 2012).

Other Anthropogenic Sources of Mortality.

Collisions with buildings are likely the second largest anthropogenic source of avian mortality, causing the deaths of millions (possibly up to 1 billion) of birds each 12

year (Loss et al., 2014). On a per building basis rural residential buildings have higher mortality rates than urban residences, but larger urban buildings seem to cause higher overall mortality (Loss et al., 2014). The number of collisions is positively correlated with the percentage of building covered by glass and the amount and height of vegetation near buildings (Klem et al., 2009). Other significant anthropogenic sources of mortality include collisions with automobiles, electrocution from power lines, poisoning from various toxins, hunting, and wind turbines (Loss et al., 2014, Klem et al., 2009).

Effects of Human-mediated Trophic Subsidies: Bird Feeders.

Bird feeding by humans constitutes a multimillion dollar industry in the US

(Fuller et al., 2008). Fuller et al. (2008) found a strong positive correlation between feeder density and avian abundance in urban centers. Leston and Rodewald (2006) found three times more fruit and birdfeeders in urban than in rural forests. Human- provided food is thought to be a major causal factor in population and life history changes (Chamberlain et al., 2009). Feeders serve as a concentrated food source and are particularly important in the winter (Brittingham & Temple, 1988). However they pose the dangers of predator attraction, collision with windows, and spread of disease

(Brittingham & Temple, 1988). Loss et al. (2014) found that residences with bird feeders had higher mortality rates from collisions with the buildings than did those without. Salmonellosis, a bacterial disease, is the most common cause of mortality at feeders, and many other diseases such as avian pox, avian mange, Coccidiosis

(gastrointestinal parasite), Aspergillosus (fungus), and Trichiomoniasis are also 13

common (Brittingham & Temple, 1998). High population density may compensate for these additional sources of mortality.

Behavioral, Physiological, and Life History Changes.

Birds undergo circadian and circannual changes in singing, migratory, reproductive, and feeding behaviors (Luniak, 2004). Dominoni et al. (2013) found that artificial light levels as low as 0.3 lux can result in earlier song and reproductive output. Artificial night light leads to the behavioral shifts of earlier song onset and night song (Nordt & Klenke, 2013). The physiological consequence of reducing melatonin release may in turn affect sleep and reproduction (Dominioni et al., 2013).

Higher levels of noise are correlated with earlier singing by serving as a wake up stimulus or resulting in a temporal shift in song to avoid the highest levels of noise

(Nordt & Klenke, 2013). Urban singing is often higher pitched, louder, and involves more twitters and pauses (Nordt & Klenke, 2013). Urban populations of European

Blackbirds (Turdus merula) exhibited a longer breeding season due to earlier gonadal growth by up to 20 days in males and 28 in females (Partecke, Van’t Hof, & Gwinner,

2005).

Anthropogenic food alters bird phenology by delaying migration and accelerating reproductive onset (Chamberlain et al., 2009). Many birds become more sedentary and overwinter in cities rather than migrate elsewhere because of milder temperatures and higher food availability (Chamberlain et al., 2009). This further increases populations and in some cases species ranges (Chace & Walsh, 2004). Bock 14

and Lepthian (1976) observed that a population of Blue Jays (Cyanocitta cristata) increased by 30% with a concomitant decrease in migratory behavior.

Although milder temperatures and higher food availability trigger earlier reproduction, the food supply is often insufficient for nestlings (Shochat et al., 2009).

Lower growth rates, slower development, and higher nestling mortality lead to lower nest success in urban populations (Shochat et al., 2010). Sauter et al. (2006) found that Florida Scrub Jays (Aphelocoma coerulescens) preferred natural food sources for nestlings. House Sparrow (Passer domesticus) nestlings in urban centers had lower body mass, indicative of nutritional stress, and showed a negative correlation between amount of plant material in diet and survival (Peach et al., 2008). The general pattern observed in urban centers is lower productivity per nesting attempt; earlier reproduction may offset this negative effect (Chamberlain et al., 2009).

Not only are food sources and consequent food selection by individuals altered in urban centers, but foraging behavior is as well. Individuals often are more aggressive and forage longer in the presence of a predator (Evans, Boudreau, &

Hyman, 2010). This combination of aggression and boldness may represent a behavioral syndrome in urban populations (Evans, Boudreau, & Hyman, 2010). In addition to these behaviors, physiological changes with regards to stress occur.

Partecke, Schwabl, & Gwinner (2006) found that urban European Blackbirds had lower corticosterone levels than individuals in forest habitats. Although individuals may adjust behaviors to minimize stress, increased human visitation to parks and other remnant vegetation patches has a negative effect on resident birds’ reproductive 15

success (Chace & Walsh, 2004). These changes point to the necessary habituation of birds living in urban centers in order to prevent overexertion and high failure rates in foraging attempts (Chace & Walsh, 2004).

Urbanization as an Ecological Trap.

Urban centers may offer benefits to birds through less extreme winters, anthropogenic food sources, and apparent lower encounters with predators. However, inhabiting urban centers may entail costs of stress, disease, low fitness, low reproductive output, and high anthropogenic structural and chemical sources of mortality. If the urban matrix constitutes poorer habitats than elsewhere, birds selecting these areas exploit an ecological trap (Leston & Rodewald, 2006). Macro and microhabitat features are commonly used cues by birds to assess habitat; consequently urban environments may draw individuals in because of dense understory and milder winter temperatures (Leston & Rodewald, 2006).

If urban habitats are more attractive, birds may nest and/or overwinter within the urban matrix despite possibly lower productivity and survival (Stracey &

Robinson, 2012). Leston & Rodewald (2006) found greater numbers of Northern

Cardinals (Cardinalis cardinalis) in urban than rural habitats (1.7 times higher in breeding season, and 4 times higher in non-breeding), as well as similar survival and productivity in adults. Stracey & Robinson (2012) found similar results in both adult and juvenile Northern Mockingbirds (Mimus polyglottos). In addition, birds did not come back to nesting areas that had low success, indicating that they were adequately selecting proper habitat (Stracey & Robinson, 2012). Shipley, Murphy, & Elzinga 16

(2013) found that within the urban matrix, edge habitats were better for producing fledglings, but constituted an ecological trap for newly post-fledgling birds. Leston &

Rodewald (2006) and Stracey & Robinson (2012) cautioned that this pattern does not hold for other species and may be reversed in migratory species in particular.

Although some general patterns emerge, it is clear that success in urban environments is variable and species-dependent.

Avian Responses to Urbanization

Urban centers differ from natural habitats through a suite of unique characteristics that have an associated set of costs and benefits. Some species thrive in urban environments, while others are unable to survive within cities. This is more complex than classification as generalist and specialist species. Diet, nesting habits, preferred habitat, migratory status, as well as other characteristics are involved. Blair

(1996) coined three response types: urban exploiters, urban adaptors, and urban avoiders.

Urban Exploiters.

Urban exploiters are species that thrive in urban environments, often to a greater extent than elsewhere; they are able to retain populations and increase abundance and density (Chace & Walsh, 2006; Husté & Boulinier, 2011). Their abundance peaks at the urban core and is negatively correlated with amount of vegetation (Kark et al., 2007). Although some endemic species may become urban exploiters, most are invasive species that have become adapted to being in close proximity with humans (Shochat et al., 2010). Intentional or accidental importation to 17

urban centers worldwide contributes to “biotic homogenization”, in which areas far apart in space become more similar in biotic components due to the loss of native and the spread of invasive species (Kark et al., 2007).

“Global homogenizers” are species that inhabit cities worldwide (McKinney,

2006). The three most well adapted species to cities globally are the House Sparrow

(Passer domesticus), European Starling (Sturnis vulgaris), and Rock Pigeon

(Columbia livia) (Savard, Clergeau, Mennechez, 2000). House Sparrows and

European Starlings are particularly aggressive competitors (McKinney, 2006). The

House Sparrow is often the most common species in urban centers (Shochat et al.,

2010).

Møller (2009) identified a number of behavioral and physiological characteristics that distinguish urban exploiters from less tolerant species. Urban exploiters have higher fear thresholds and shorter flight distances when avoiding a predator, which denote risk taking behavior (Møller, 2009). A larger Bursa of

Fabricius was also associated with these individuals; indicating a stronger immune system capable of withstanding greater physiological stress (Møller, 2009). Rump and tail feathers are less easily removed in urban species, which suggests low predation selection because loose tail feathers are an adaptation for escaping predators (Møller,

2009). Many of these species are also granivores and omnivores, consuming and depending on anthropogenic food sources (Kark et al., 2007; McKinney, 2002).

Behavioral plasticity is a major requirement for urban exploitation; Sol et al.

(2005) found that plasticity was correlated with larger brain size. This enables urban 18

exploiters to utilize anthropogenic food sources through feeding innovations

(exploring and developing novel feeding methods through problem solving and complex learning) (Kark et al., 2007; Møller, 2009). One example of this is House

Sparrows feeding on insects in radiator grilles of cars (Lefebvre et al., 1997).

At the population level, urban exploiters have larger breeding ranges, a greater tendency for dispersal, more reproductive bouts per season, higher fecundity and adult survival rates, and are more gregarious and sedentary (Kark et al., 2007; Møller,

2009). Many of these species are cliff and cavity nesters- nesting on rocks and buildings; this is evident in names like House Sparrow and Chimney Swift

(McKinney, 2006).

Urban Adaptors.

This type is less well defined, but these species peak in abundance in the suburbs (McKinney, 2006). Urban adaptors exhibit some degree of behavioral plasticity that allows them to exist simultaneously in both urban and rural areas (Wang et al., 2008). These species are capable of living in moderately urbanized areas (Husté

& Boulinier, 2011). Suburbs represent a switchpoint from native, often woodland species to invasive and exotic urban species (Blair & Johnson, 2008). These are areas of moderate disturbance and woodland edges. Although they are usually non- migratory these species are often native early successional species and edge specialists

(McKinney, 2002; McKinney, 2006).

Highly productive green lawns in combination with anthropogenic food sources allow more feeding and nesting guilds to persist than in more urbanized areas 19

(McKinney, 2002). Omnivores, ground foragers, and aerial insectivores are common here; feeders and seeds of ornamental seeds provide food for the former, and open lawns, pavement, and lights enable easy access to insects for the latter (McKinney,

2002). Tree, shrub, and cavity nesters are also common (Johnston, 2001). Chace et al.

(2002) observed that Brown-headed Cowbirds (Molothrus ater) in Boulder, Colorado moved from Ponderosa Pine and riparian habitats in the morning towards more urban areas in the afternoon and evening. Other urban adaptors include the American

Robin (Turdus migratorius), Blue Jay (Cyanocitta cristata), swifts, and finches

(McKinney, 2002). Suburban areas encompass greater amounts of green space and thus allow for moderately tolerant species to persist that do not rely singularly on anthropogenic food sources (McKinney, 2002; Chamberlain et al., 2009).

Urban Avoiders.

Urban avoiders require natural food sources and undisturbed areas, are typically old growth forest interior species and tree-foraging insectivores, and peak in abundance well outside of urban areas (McKinney, 2002; McKinney, 2006). These species are often specialized in habitat, diet, and nest type, and so cannot inhabit drastically different urban environments. Migration might be the most important life history trait determining sensitivity to urbanization (Whitcomb et al., 1981).

Neotropical migrants that specialize in forest interior habitats, make open nests on or near the ground, and have low reproductive potential make up the most sensitive taxa

(Whitcomb et al., 1981). 20

Friesen, Eagles, & Machay (1995) found that 4 hectare woodlots in rural areas had higher diversity and abundance of neotropical migrants than 25 hectare woodlots in urban areas, highlighting the importance of intact, isolated forest patches for urban avoiders. MacGregor-Fors, Perez, & Schondube (2010) found that the abundance of

Neotropical migrants was positively related to tree number and negatively related to human density. Open nests on or near the ground would be very vulnerable to predation by domestic cats and dogs (Canis lupis familiaris) and trampling by humans in urban environments (Kark et al., 2007). Most urban avoiders breed once each season and have lower reproductive output than urban exploiters and urban adaptors that breed multiple times each season (Blair & Johnson, 2008). This competition may be amplified by later establishment of breeding territories and reproduction of migrants; nesting sites in more developed areas may already be taken by resident species (Blair & Johnson, 2008).

Nest predation has a major negative effect on songbird populations (Chace et al., 2002). High abundances of cats and Gray Squirrels (Sciurus carolinensis) in urban areas as well as increased nest parasitism by edge specialists like cowbirds may prevent neotropical migrants from entering any habitat other than isolated forests

(Friesen, Eagles, & Mackay, 1995). Low stress tolerance to human activity is also very likely to play a major role (Friesen, Eagles, & Mackay, 1995). Urban avoiders include species such as the Empidonax flycatchers, Red-eyed Vireo (Vireo olivaceus), and Cerulean Warbler (Setophaga cerulea) (Chace & Walsh, 2006). 21

General Trends.

The three types of avian responses are not necessarily mutually exclusive, but they illustrate some general patterns in community changes from rural to urban areas.

First, urbanization favors resident over migrant species (Møller, 2009). Second, mostly rock and cavity nesters are found in cities while more urban areas encompass ground nesters (Møller, 2009). Species that nest in dead trees, like most woodpeckers, also decline in more urbanized areas because dead trees are usually quickly cut down

(Kark et al., 2007). Third, granivorous and omnivorous species are selected for in urban areas over insectivores (McKinney, 2002; Chace & Walsh, 2006; Kark et al.,

2007). Perhaps most importantly, communities become more homogeneous going from rural to urban environments, contributing to local extinctions and lower diversity

(McKinney, 2006).

Previous Research and Predictions

Because of the potential for drastic changes and negative effects on urban avifauna, quantification of community characteristics is essential for proper management. The rural to urban gradient is a common approach to analyzing the effects of urbanization (McKinney, 2006). Studies have been conducted surrounding cities on a global scale, and several patterns have emerged in addition to those previously discussed.

Connor and McCoy’s (1979) random sampling hypothesis suggested that diversity would be higher in cities because various species from surrounding regions would congregate. This has been proven incorrect because of the physiological and 22

life history traits required for success in urban environments (Shochat, Lerman, &

Fernandez-Juricic, 2010). Conversely, the general pattern observed is that urban areas have lower diversity than rural areas (reviewed in Chace & Walsh, 2006; McKinney,

2006; Chamberlain et al., 2009). Species may show a gradient of decreasing diversity from rural to urban settings, or alternatively increased diversity between the two extremes (Blair, 1996).

The intermediate disturbance hypothesis predicts that the greatest diversity will be found in areas of moderate development (i.e. suburbs), due to a balance of biotic and abiotic limitations, and fewer competitive and dominant (high abundance) species

(Blair, 1996). Biotic limitations largely control presence and abundance in rural areas, and physical limitations largely control presence and abundance in urban areas

(McDonnell et al., 1997). Despite the increased habitat heterogeneity that suburbs and other moderately developed areas represent, 31 of 51 studies (61%) analyzed by

Marzluff, Bowman, & Donnelly (2001) showed lower diversity in these areas than in rural settings.

Much of this research has been conducted in North American Eastern

Deciduous Forest habitats, which have a longer history of avian research and urban development (Hansen & Urban, 1992). Hansen and Urban (1992) found Eastern

Deciduous Forest species to be more sensitive to landscape changes than Pacific

Northwest species; edge effects are stronger and there are more migrants in eastern deciduous forest.

Current Project

23

Project Goals.

The present study involves sampling bird species across a gradient of urbanization in a central hardwood forest ecosystem centered in Athens, Ohio. The gradient has sites ranging from a low to high imperviousness index. I propose to address three hypotheses.

First, I hypothesize that avian diversity should be lowest in the highest urbanized areas and highest in rural (least disturbed) areas. This would agree with numerous previous studies. For example, Clergeau et al. (1998) found patterns of decreasing diversity from urban to rural in both Quebec, Canada (eastern deciduous forest) and the more warmer and agricultural Rennes, France.

Second, the abundances of species should differ among habitats that vary in urbanization. One hypothesis is that invasive and generalist species will be more abundant in urbanized areas, and sensitive and specialist species will be more abundant in less disturbed areas. Blair and Johnson (2008) found this pattern in

Oxford, Ohio, Saint Paul, Minnesota, and Palo Alto, California. Clergeau et al. (1998) also found a gradient of decreasing dominance of House Sparrow, European Starling, and Rock Pigeon from urban to rural areas in both Quebec City, Canada and Rennes,

France (Clergeau et al., 1998). Loss, Ruiz, and Brawn (2009) found a positive relationship of proportion of undeveloped land with both species richness and density of native birds in Chicago, Illinois. Native and migratory species increased and exotic and non-migratory species decreased in densities with increasing undeveloped land

(Loss, Ruiz, & Brown, 2009). 24

Third, I hypothesize that avian communities in urban habitats are unique from rural, least developed habitats. There should be a low percent similarity between these two extremes in species composition and guild structure, due to presence of urban exploiters versus urban avoiders. As discussed previously, nesting guilds have been found to change from including ground nesters to predominately rock and cavity nesters (Møller, 2009), and feeding guilds change from including insectivores to predominately granivores and omnivores going from a rural to urban gradient (Chace

& Walsh, 2006; McKinney, 2006; Kark et al., 2007).

Project significance

Athens, Ohio is a small city of approximately 23,800 people (US Census

Bureau, 2014). Rather than isolated green patches within a larger urban and suburban matrix as in most previous studies, Athens is an urban matrix surrounded by central hardwood deciduous forest. Consequently, the results of this study may significantly differ from those of previous studies in that the Athens urban community may be more encompassing in terms of species richness and abundance.

A major goal of this project is to expand the results of this study from the local level to a broader scale of urbanization across the globe. Avian diversity is an indicator of a city’s ecological and social health. Changes in diversity have ecological and social implications for habitat management. City planners may need to take greater action to improve avian diversity.

Avian diversity and community assessment can be used in combination with vegetation and habitat data to locate areas of high biodiversity for preservation, and 25

devise efforts for extermination of invasive species and propagation of native species

(McKinney, 2002; Loss, Ruiz, & Brown, 2009). This compromises reconciliation ecology, wherein habitats altered by development are spatially arranged, designed, and managed in a way that promotes maximum diversity, ecosystem services, and economic benefits (Grimm et al., 2008). Solutions must create favorable conditions for native species by integrating dominant and subordinate species evolutionary differences (Savard, Clergeau, & Mennechez, 2000). This can be done by bottom-up actions such as tree plantings and nest box construction and placement, and top-down actions involving city planning and public works (Savard, Clergeau, & Mennechez,

2000; Melles, 2005).

Human perception is critical to enhancing and maintaining urban diversity, as exposure to wildlife dramatically influences public support of conservation efforts

(Melles, 2005). Sixty-one percent of the world’s population is expected to live in urban spaces by 2030, at which point a state of “biological poverty” could ensue

(Melles, 2005). Hence, maintaining or improving avian diversity in cities has implications for public health, wildlife management, and human-wildlife interactions in an increasingly urbanizing world (French, 2012).

Avian diversity is heavily and negatively influenced by urbanization. An analysis of avian diversity in Athens, Ohio will serve as an ecological and social health assessment for the city as a whole. It will also contribute to knowledge of urban ecosystems and their effect on native flora and fauna within and surrounding cities. 26

Methods Data Collection

I sampled four sites of varying area, distance from the urban core, and surface imperviousness indices (Table 1). Area was defined as the amount of continuous green space bordered by impermeable surface. Area and distance from the urban core were determined using Google Maps and ACME Planimeter. These sites were a mix of grassland and forest edge habitats: a park at the city’s center, two locations on the periphery (referred to from this point as Community Center and West State Street sites), and one isolated, rural site outside of the urban matrix (Radar Hill) (Appendix

A).

Following the protocol of Huff et al. (2000), for each site a 200 meter transect was located at least 50 meters away from the edge of the green space and contained 3 points at 100 meter intervals. Following a 5 minute period of acclimation to my presence, birds were recorded through visual and auditory observation in a 100 meter radius from each point for 15 minutes.

I attempted to avoid record duplications of individuals between points by best judgment given previous observation location and observed movements of individuals.

I recorded the sex and age along with behavior (flying over, flocking, etc.) when suitable field marks were observed. The presence and identity of potential predators were recorded. Weather conditions (cloud cover and temperature) were also recorded.

Surveys were performed on days with little to no precipitation and little to no wind.

Information was recorded on a data sheet and then transferred to an Excel spreadsheet. 27

Surveys were taken at 3 different times of the morning: 07:00, 09:00, and

11:00, following the protocol of Finnicum (2012). Surveys were conducted between

September 3rd and December 11th, 2013. Each site was sampled 5 times for each time slot, giving me a sample size of n=15 for each site and N=60 for all sites totaled.

Data Analysis

Imperviousness indices were calculated using the protocol of Finnicum (2012).

Satellite photographs from Google Maps and AMCE Planimeter were standardized to a 200 meter scale with sites centered in the photographs (Appendix B). A 264 cross grid was placed over each photograph using Image J, and percent impervious surface was calculated by dividing the number of crosses that fell over impervious surface over the total number of crosses.

Bird species were classified to nesting and feeding guild following the definitions of Cornell University (2011). I classified urban exploiters as species found only in the urban site or species previously known to be urban exploiters (Savard,

Clergeau, Mennechez, 2000). I classified urban adaptors as species found in combinations of 2-4 sites. I classified urban avoiders as species found only in the rural site.

All data analyses were performed using the statistics program R. The package

Vegan: ecological diversity was used for these avian community analyses, and formulas are as given in Oksanen, 2013.

I tested my first and second hypotheses using species richness and abundance through the Shannon-Weiner (H') and Simpson Diversity Indices (D1) to compare 28

diversity between the 4 sites. I compared species diversity among sites using T-tests to determine whether the sites were significantly different.

∑

∑

Where pi= the abundance of individuals of one species divided by total avian

abundance.

Total and average species richness were calculated for each site.

Species evenness, a measure of how similar species’ abundances are, for each site was found using Pielou’s evenness index (J).

Where H'= Shannon-Weiner Index, and S= species richness.

Rank abundance curves were generated for each site by finding the percent of total sightings each species represented and ranking them on a logarithmic scale using

Microsoft Excel. Invasive species were excluded so that abundances’ of the native communities were not masked.

Species accumulation curves were generated for each site to assess the likelihood of actual total species richness of each site having been reached through sampling efforts using Kindt’s exact accumulator ( ̂ ).

̂ ∑

29

where , where fi is the frequency of species i, N= abundance and

species richness data from all samples, and n= random subset of samples.

Bootstrap and Abundance-based Coverage Species Richness Estimators (Sp) were used to further estimate community size.

∑

Where So= number of observed species, pi= proportional abundances of

species, and N= number of sites.

∑

Where Sabund= the number of species that occur over 10 times in sampling, Srare= the number of species that occur 10 or fewer times in sampling, f1= the number of species

that occur 1 time in sampling, a1= number of species occurring in only 1 site, ai= the

number of species with abundance i,

To assess my third hypothesis I calculated Bray-Curtis dissimilarity (bii′), a measure of difference as distance between species according to similarity in sites occupied. A non-metric multidimensional scaling was used to visualize the site differences in species space.

∑ | |

30

Where i and i ′ are samples, nij, ni ′j= single species abundances, ni+, ni ′+=

sample total abundances

Guild differences were assessed following the protocol of Culbert et al. (2013).

I created a univariate model using species richness of each guild and site area, distance from urban core, and imperviousness index to run a series of regressions and

ANOVAs.

Results Species Richness, Abundance, Diversity, and Evenness

A total of 2,852 detections of 49 species were recorded over the survey period.

The most rural site had the greatest total species richness (36 species), followed by

West State Street (33 species), Community Center (31 species), and the most urban with the lowest (23 species) (Figure 1). The West State Street site had the highest average species richness per sample (12.8±0.712), followed by the rural site

(12.4±0.767), Community Center (10.7±0.573), and urban (8±0.762) (Figure 2).

Four species were classified as urban exploiters, 39 as urban adaptors, and 7 as urban avoiders (Table 2). Fifteen species were observed in all four sites; all were common permanent residents. Chipping Sparrows (Spizella passerina) and one

Brown Creeper (Certhia americana) were found only in the urban site. A Black-and-

White Warbler (Mniotilta varia), Chestnut-sided Warbler (Setophaga pensylvanica),

Blackburnian Warbler (Setophaga fusca), two Blue-gray Gnatcatchers (Polioptila caerulea), two Nashville Warblers (Oreothlypis ruficapilla), and two Yellow-throated

Warblers (Setophaga dominica) were found only in the rural site. 31

The most common species were the European Starling (785 detections) and

Cedar Waxwing (Bombycilla cedrorum) (378 detections). Song Sparrows (Melospiza melodia), Common Grackles (Quiscalus quiscula), American Goldfinches (Spinus tristis), Carolina Chickadees (Poecile carolinensis), Blue Jays (Cyanocitta cristata),

Northern Cardinals (Cardinalis cardinalis), and American Robins (Turdus migratorius) also had 100 or more detections. The most rare species were the Black- and-White Warbler, Chestnut-sided Warbler, Blackburnian Warbler, Blue-gray

Gnatcatcher, Nashville Warbler, Yellow-throated Warbler, Brown Creeper, Common

Yellowthroat (Geothlypis trichas), Eastern Kingbird (Tyrannus tyrannus), Yellow- bellied Sapsucker (Sphyrapicus varius), Summer Tanager (Piranga rubra), and Indigo

Bunting (Passerina cyanea), with 1-2 detections.

The rural site had the highest number of migrant species (13) and the urban site had the least (5) (Figure 3). The proportion of detections that were invasive species was highest at the Community Center site (54%) and lowest at the rural site (7.73%)

(Figure 4).

Shannon-Weiner and Simpson indices that were calculated with species richness and abundance showed the greatest diversity at the West State Street site, followed by the rural, Community Center, and the lowest diversity at the urban site

(Table 3). This pattern was the same whether migrants were included or excluded.

The Shannon-Weiner value for the rural site was significantly greater than that of the urban site (t=-2.94, p<0.05). The Shannon-Weiner value for West State Street site 32

was significantly greater than that of the urban site (t=2.86, p<0.05). All other comparisons were nonsignificant.

Pielou’s species evenness that was calculated from the Shannon-Weiner Index values and species abundances was high and similar between sites (Table 4). There were no significant differences between sites when migrants were included or excluded. The rank abundance curves for the urban, West State Street, and

Community Center sites leveled off slower than that of the rural site; the rural site had most species at low abundance (Figures 6-8).

Predator Presence

Predator observations varied in frequency and type by site. Domestic cats were observed at the urban and Community Center sites, while the West State Street and rural sites were dominated by avian predators. The West State Street had the highest frequency of predator observations, followed by the Community Center, with the lowest frequency at the urban and rural sites (Table 5).

Species Accumulation Curves and Number of Unobserved Species

The species accumulation curves for each site approached a plateau. This indicates that most if not all species present in each site were observed and that the sampling efforts were sufficient, because the increase in number of species (y-axis) with samples (x-axis) has almost leveled off (Figures 9-12). Approximately 11 species may have been unobserved with all sites combined based on the Bootstrap

Species Richness Estimator (Table 6). The urban site may have had up to 4 33

unobserved species, the Community Center site 13, the West State Street site 5, and the rural site 2 (Figure 13).

Species Differences by Site Nonmetric Multidimensional Scaling

When sites were plotted within a species space Nonmetric Multidimensional

Scaling, differences in sites emerged. Sites overlapped to an extent, but the rural,

West State Street, and Community Center had more overlap with each other than any did with the urban site (Figure 14). The rural site had notably more Field Sparrows

(Spizella pusilla) and Yellow-rumped Warblers (Setophaga coronata). The West

State Street site was more distinguished by the presence of Summer Tanagers and

Indigo Buntings, and the Community Center by Willow Flycatchers (Empidonax traillii), Eastern Kingbirds, and Common Yellowthroats. The urban community was more defined by House Sparrows and Chipping Sparrows. The rural community and urban community were most diverged from each other.

Guild Univariate Model

Ground nester richness was positively correlated with area (F=79.7, t=8.927, p<0.05) (Figure 15). Cavity nester richness was positively correlated with distance from the urban core (F=152.96, t=12.37, p<0.05) (Figure 16). Building nester richness was negatively correlated with imperviousness index (F=31.224, t=-5.588, p<0.05) (Figure 17). Granivore richness was positively correlated with imperviousness index (F=31.224, t=5.588, p<0.05) (Figure 18). All other correlations were nonsignificant. 34

Discussion

I found apparent differences in the passerine and near passerine community along a gradient from the rural surroundings to the urban matrix of Athens, Ohio.

Avian diversity was lowest in the urban and highest in the rural site and abundances of species differed among habitats.

Species richness was much lower in the urban site than in the other sites. This may be attributed to the presence of more migrant species in the other sites, especially the rural site. While migrants made up only 21.7% of species observed in the urban sites, 36.1% of species observed in the rural site were migrants. No warbler species were observed in the urban site, 6 out of 8 warbler species were only observed in the rural site, 6 out of the 7 urban avoiders were warblers, and all warbler species were infrequently detected in the rural, West State Street, and Community Center sites.

Most wood warblers have suffered significant declines throughout North America

(Stewart, 1987), and are intolerant of urban areas (MacGregor-Fors, Morales-Pérez, &

Schondube, 2010). My results highlight this group’s sensitivity and the importance of maintaining undisturbed habitat.

None of the 15 species common to all four sites were migrants, but all 12 rare species were migrants. The abundance of migrants did not decrease going from the rural to urban site, but the species richness of migrants did. The decrease in richness agrees with previous studies (MacGregor-Fors, Morales-Pérez, & Schondube, 2010).

Whitcomb et al. (1981) had suggested that neotropical migration is the most important trait in determining sensitivity to urbanization. Both Whitcomb et al. (1981) and 35

MacGregor-Fors, Morales-Pérez, & Schondube (2010) stated that lack of forest vegetation largely contributes to the absence of many neotropical migrants in urban environments, and the imperviousness indices of the sites indicate this.

As migrants decreased going from rural to urban sites, invasive and exotic species increased, also agreeing with previous studies (McKinney, 2006; Møller,

2009). Observations of urban exploiters follow similar patterns as previous studies

(Blair, 1996; Savard, Clergeau, Mennechez, 2000; Shochat et al., 2010). Seventy-five of the 83 detections of House Sparrows were in the urban site and none were in the rural site. House sparrows are most common in urban environments (Shochat et al.,

2010). European Starlings had the most detections in the urban and city periphery sites, consistent with their status as an urban exploiter and aggressive competitor

(McKinney, 2006). Although Rock Pigeons were only observed at the Community

Center site, I frequently observed them during non-surveying times at the urban core.

Chipping Sparrows and Brown Creepers were only found in the urban site.

However, these are not urban specialists given their open woodland and forest habitat requirements (Cornell University, 2011) and low numbers of detection (6 and 1).

They likely represent under sampled species still present in other sites. Brown

Creepers have similar calls to Golden-crowned Kinglets (Regulus satrapa), and their small size and cryptic coloration makes them difficult to observe (Cornell University,

2011).

Species diversity was significantly lower in the urban than rural site as predicted by my first hypothesis. Although nonsignificant, the higher diversity of the 36

West State Street than the rural site supports the intermediate disturbance hypothesis

(Blair, 1996). The combination of intermediate levels of vegetation and impermeable surfaces represent habitat heterogeneity that should support a number of urban adaptable species as well as being the interface between urban exploiter and urban avoider dominance (Blair, 1996; McDonnell et al., 1997). The majority of species were found in 2-3 sites, which suggests that much of the avian community in and surrounding Athens is composed of urban adaptors.

Other feeding and nesting guild results are consistent with previous studies

(McKinney, 2002; Chace & Walsh, 2006; Kark et al., 2007; Møller, 2009). Ground nester richness increased with increasing area. The rural site had the largest area of uninterrupted green space and ground nester richness was higher compared to the other sites. Ground nesters are highly vulnerable to disturbance and predation by humans and domestic dogs and cats (Kark et al., 2007), and these results suggest this vulnerability as a limiting factor.

Cavity nester richness increased with increasing distance from the urban core.

Woodpeckers are cavity nesters which generally are less common in urban areas (Kark et al., 2007). The Downy Woodpecker (Picoides pubescens) was the only woodpecker present in the urban site; the Pileated Woodpecker (Dryocopus pileatus) was classified as an urban avoider. Decaying trees are cut down in urban areas and larger woodpeckers such as the Pileated Woodpecker and Northern Flicker (Colaptes auratus) require larger snags in forested areas (Blewett & Marzluff, 2005). However, a greater proportion of total species in the urban and Community Center sites were 37

cavity nesting species (Møller, 2009). Shrub nesters were most common in the two city periphery sites, possibly due to the high abundance of intermediate height vegetation in suburban areas.

Building nesters utilize human-made structures for nest building and include species like the Rock Pigeon. The decrease in building nester richness with imperviousness index was unexpected. However, this may have been due to low building nester richness (3 species), and because two of these species (Eastern Phoebe

(Sayornis phoebe) and Chimney Swift (Chaetura pelagica)) are insectivorous

Neotropical migrants.

Different feeding guilds showed variable responses to changes in habitat variables. Granivores significantly increased with greater impermeable surface. This is likely because these species are better able to utilize anthropogenic food sources like bird feeder seed and garbage than other guilds (Chace & Walsh, 2006). The proportion of species that were omnivores did not greatly increase going from the rural to urban site. Both the richness and proportion of insectivorous species decreased, although not significantly correlated with any of the three variables. The severe decline of insectivorous species with urban development has been a common trend due to the specialization in traits of many insectivores, and the high proportion of migrants that are insectivores (McKinney, 2002). Feeding guild patterns are consistent with previous studies (McKinney, 2002; Chace & Walsh, 2006; McKinney,

2006; Kark et al., 2007; Møller, 2009). 38

The species accumulation curves in total and for each site and small number of possible unobserved species predicted by the Bootstrap and Abundance-based

Coverage Species Richness Estimator indicate that my sampling design was sufficient and this data is likely reliable. This study was conducted over migration, but diversity and species accumulation results were unchanged when migrants were excluded from analyses.

The differences, although nonsignificant, in richness, diversity, and guild composition between the two urban periphery sites indicate that the West State Street site is more similar to the rural site and the Community Center site is more similar to the urban site. This may be due to predator and nest space availability differences between the two sites. Cats were the only predator observed in the Community Center site, while raptors were the only predators observed in the West State Street site. The higher imperviousness index and nesting opportunities due to buildings near the

Community Center site may have allowed invasive species and cavity nesters such as

European Starlings and House Sparrows to better colonize the area.

Although obvious differences were seen in richness and diversity as well as in other factors going from the rural to urban site, Athens is a small urban center surrounded by forest and this is reflected in the patterns I observed. The percent impervious surface at the urban center was still under 50%. Species evenness was high in all sites. Many native species, including sensitive taxa such as Brown

Creepers were present in the urban site. Invasive species still made up less than 50% of detections in the urban site. Although European Starlings had the highest 39

abundance by detection rate, Cedar Waxwings were also detected in high numbers in every site.

Much of the current literature on the effects of urbanization on avifauna focuses on large urban centers. More research on smaller urban centers similar to

Athens as well as urban centers of intermediate sizes would provide greater insight on how tolerant different species are of development as well as how cities can be designed to promote greater avian richness and diversity.

Future studies that take place over a longer time period and wider area and scope, as well as duplicating this analysis in additional small urban centers will allow for better assessment of the role of urbanization in human-dominated landscapes. A longer surveying period encompassing spring migration would include more migrants and hence likely show greater total richness. More transects at more sites would result in a broader and more thorough assessment of the passerine and near passerine community in and surrounding Athens. Incorporating more variables such as nestling production, fledgling success, and adult body condition, as well as monitoring food sources and feeding habits would allow further insight into the community and the effects of development.

The results of this study carry significance for urban conservation ecology and city planning. Urban conservation ecology involves using the evolutionary differences between species found in urban and rural habitats to design better habitat for urban adaptors and even urban avoiders (Shochat et al., 2010). The results of this study can be integrated into urban planning to maintain and improve green spaces (Savard, 40

Clergeau, & Mennechez, 2000) to support and increase the abundance of native and sensitive species such as Brown Creepers abundances.

With over half the world’s population living in urban centers today and the number rising, city dwellers’ perceptions of nature are critical to conservation efforts

(Savard, Clergeau, & Mennechez, 2000). Maintaining biodiversity helps to foster a healthy definition of nature in the minds of individuals, which in turn leads to a better awareness of ecological health and support for environmental issues (Melles, 2005).

The results of this study, although limited in scope, show that while urban development has had a negative effect on the native avifauna of Athens, the effect appears less than that of larger urban centers. Assessment and identification of factors that permit native species to utilize urban environments may be used in combination with research from other urban centers to develop more sustainable and biologically diverse cities.

41

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Figures Legend

Figure 1: Total species richness (all samples combined) by site.

Figure 2: Average species richness per sample by site at a 95% confidence interval.

Figure 3: Total species richness for each site of permanent resident species and migrant species.

Figure 4: Total invasive species and native species detections (all samples combined) for each site.

Figure 5: Rank abundance curve, on a logarithmic scale, for the urban site.

Figure 6: Rank abundance curve, on a logarithmic scale, for the Community

Center site.

Figure 7: Rank abundance curve, on a logarithmic scale, for the West State

Street site.

Figure 8: Rank abundance curve, on a logarithmic scale, for the rural site.

Figure 9: The species accumulation curve for the urban site. The number of species are plotted on the Y axis against the number of visits to the urban site.

Figure 10: The species accumulation curve for the Community Center site. The number of species are plotted on the Y axis against the number of visits to the

Community Center site.

Figure 11: The species accumulation curve for the West State Street site. The number of species are plotted on the Y axis against the number of visits to the

West State Street site. 51

Figure 12: The species accumulation curve for the rural site. The number of species are plotted on the Y axis against the number of visits to the rural site.

Figure 13: Species richness based on the Abundance-based Species Estimator for each site with standard error.

Figure 14: NMDS showing site differences in species space.

Figure 15: Plot of ground nester species richness against area.

Figure 16: Plot of cavity nester species richness against distance from the urban core.

Figure 17: Plot of building nester species richness against index of imperviousness.

Figure 18: Plot of granivore species richness against index of imperviousness.

52

Figures

Figure 1

Figure 2 53

Figure 3

Figure 4 54

Figure 5

Figure 6 55

Figure 7

Figure 8

56

Figure 9

Figure 10 57

Figure 11

Figure 12 58

Figure 13

Figure 14 59

Figure 15

Figure 16 60

Figure 17

Figure 18 61

Tables

Table 1: Area, distance from urban center, and imperviousness index by site.

Urban Community West State Rural Center Area (km2) 0.051 0.126 0.356 2.327 Distance from 0.160 2.770 1.642 1.867 Urban Center (km2) Index of 48.9 48.3 31.1 23.5 Imperviousness (%)

62

Table 2: List of species observed, feeding and nesting guilds, urban response type classification, total number of detections (Detect No.), and sites observed in. Adaptor= Urban adaptor, Avoider= Urban avoider, Exploiter= Urban exploiter. * denotes that classification was based on previous observations and classification (Savard, Clergeau,

Mennechez, 2000; Cornell University, 2011). UR=Urban, CC=Community Center, WS= West State Street, RU=Rural.

Species Feeding Guild Nesting Classification Detect UR CC WS RU Guild No. American Goldfinch Spinus tristis Granivore Shrub Adaptor 105 Y Y Y Y American Crow Corvus brachyrhynchos Omnivore Tree Adaptor 90 Y Y Y Y American Robin Turdus migratorius Insectivore Tree Adaptor 172 Y Y Y Y Black-and-White Warbler Mniotilta varia Insectivore Ground Avoider 1 N N N Y Blackburnian Warbler Setophaga fusca Insectivore Tree Avoider 1 N N N Y Blue-gray Gnatcatcher Polioptila caerulea Insectivore Tree Avoider 2 N N N Y Blue Jay Cyanocitta cristata Omnivore Tree Adaptor 133 Y Y Y Y Brown Creeper Certhia Americana Insectivore Tree Adaptor* 1 Y N N N Carolina Chickadee Poecile carolinensis Omnivore Cavity Adaptor 124 Y Y Y Y Carolina Wren Thryothorus ludovicianus Insectivore Cavity Adaptor 84 Y Y Y Y Cedar Waxwing Bombycilla cedrorum Frugivore Tree Adaptor 378 Y Y Y Y Chestnut-sided Warbler Setophaga pensylvanica Insectivore Shrub Avoider 1 N N N Y Chimney Swift Chaetura pelagica Insectivore Building Adaptor 60 Y N Y Y Chipping Sparrow Spizella passerine Granivore Shrub Adaptor* 6 Y N N N Common Yellowthroat Geothlypis trichas Insectivore Shrub Adaptor 1 N Y N N Common Grackle Quiscalus quiscula Omnivore Tree Adaptor 100 Y Y Y Y Dark-eyed Junco Junco hyemalis Granivore Ground Adaptor 43 Y N N Y Downy Woodpecker Picoides pubescens Insectivore Cavity Adaptor 34 Y Y Y Y Eastern Bluebird Sialia sialis Insectivore Cavity Adaptor 46 Y Y Y Y 63

Species Feeding Guild Nesting Classification Detect UR CC WS RU Guild No. Eastern Kingbird Tyrannus tyrannus Insectivore Tree Adaptor 1 N Y N N Eastern Phoebe Sayornis phoebe Insectivore Building Adaptor 6 N N Y Y Eastern Towhee Pipilo erythrophthalmus Omnivore Ground Adaptor 5 N Y N Y European Starling Sturnus vulgaris Insectivore Cavity Exploiter* 785 Y Y Y Y Field Sparrow Spizella pusilla Insectivore Ground Adaptor 3 N N Y Y Golden-crowned Kinglet Regulus satrapa insectivore Tree Adaptor 7 Y N Y Y Gray Catbird Dumetella carolinensis Insectivore Shrub Adaptor 26 N Y Y Y House Finch Haemorhous mexicanus Granivore Tree Exploiter* 20 Y Y Y Y House Sparrow Passer domesticus Granivore Cavity Exploiter* 83 Y Y N N House Wren Troglodytes aedon Insectivore Cavity Adaptor 3 N Y N N Indigo Bunting Passerina cyanea Insectivore Shrub Adaptor 1 N N Y N Mourning Dove Zenaida macroura Granivore Tree Adaptor 17 Y Y Y N Nashville Warbler Oreothlypis ruficapilla Insectivore Ground Avoider 2 N N N Y Northern Cardinal Cardinalis cardinalis Granivore Shrub Avoider 153 Y Y Y Y Northern Flicker Colaptes auratus Insectivore Cavity Avoider 14 N N Y Y Northern Mockingbird Mimus polyglottos Omnivore Shrub Avoider 45 N Y Y Y Pileated Woodpecker Dryocopus pileatus Insectivore Cavity Avoider 6 N N N Y Red-bellied Woodpecker Melanerpes carolinus Insectivore Cavity Avoider 10 N Y Y Y Red-winged Blackbird Agelaius phoeniceus Insectivore Shrub Avoider 5 N Y Y Y Rock Pigeon Columbia livia Granivore Building Exploiter* 10 N Y N N Song Sparrow Melospiza melodia Insectivore Scrub Adaptor 130 Y Y Y Y Summer Tanager Piranga rubra Insectivore Tree Adaptor 1 N N Y N Tufted Titmouse Baeolophus bicolor Insectivore Cavity Adaptor 41 Y Y Y Y White-breasted Nuthatch Sitta carolinensis Insectivore Cavity Adaptor 26 Y N Y Y White-crowned Sparrow Zonotrichia leucophrys Insectivore Ground Adaptor 3 N Y Y N White-throated Sparrow Zonotrichia albicollis Granivore Ground Adaptor 14 N Y Y Y 64

Species Feeding Guild Nesting Classification Detect UR CC WS RU Guild No. Willow Flycatcher Empidonax traillii Insectivore Shrub Adaptor 2 N Y Y N Yellow-bellied Sapsucker Sphyrapicus varius Insectivore Cavity Adaptor 1 N Y N N Yellow-rumped Warbler Setophaga coronate Insectivore Tree Adaptor 20 N N Y Y Yellow-throated Warbler Setophaga dominica Insectivore Tree Avoider 2 N N N Y 65

Table 3: Shannon-Weiner and Simpson’s diversity indices including and excluding migrant birds. UR= Urban, CC= Community Center, WS= West State

Street, RU= Rural.

Site Including Migrant Birds Excluding Migrant Birds Shannon- Simpson Shannon-Weiner Simpson Weiner Mean Max Mean Max Mean Max Mean Max

UR 1.596 2.000 0.714 0.833 1.496 2.363 0.699 0.895 CC 1.711 2.405 0.688 0.900 1.641 2.405 0.675 0.900 WS 2.044 2.673 0.784 0.920 1.960 2.535 0.775 0.907 RU 2.004 2.554 0.785 0.915 1.866 2.476 0.759 0.907

Table 4: Pielou’s evenness values for the four sites including and excluding migrants; where 1= even (all species at the same abundance), and 0= uneven (no species at the same abundance).

Pielou’s Evenness

Site Including Migrants Excluding Migrants

Mean Max Mean Max

Urban 0.799 0.935 0.815 0.951

Community 0.717 0.938 0.713 0.938 Center

West State 0.801 0.964 0.807 0.959 Street

Rural 0.807 0.968 0.798 0.965

66

Table 5: Predator detections by site.

Site Species Seen Average number observed per visit Urban Felis catus, Accipiter cooperii 0.2 Community Center Felis catus 0.67 West State Street Buteo jamaicensis, Buteo 0.8 lineatus Rural Buteo lineatus 0.2

Table 6: The estimated number of unseen species when all sites were combined using the Bootstrap Species Richness Estimator.

Number of Observed Plus Variance Observed Estimated Species Unseen Species

49 54.25 3.21

67

Appendices

Appendix A: Photographs of Study Sites

Image 1: urban site. 68

Image 2: Community Center site. 69

Image 3: West State Street site. 70

Image 4: Rural site.

Appendix B: Google Maps/ACME Planimeter Satellite Images of Study Sites

Image 1: urban site, 48.9% impervious surface 71

Image 2: Community Center site, 48.3% impervious surface

Image 3: West State Street site, 31.1% impervious surface 72

Image 4: rural site, 23.5% impervious surface