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SOIL ECOLOGY ALONG AN URBAN TO RURAL GRADIENT IN THE SOUTHERN APPALACHIANS by MITCHELL A. PAVAO-ZUCKERMAN (Under the Direction of David C. Coleman) ABSTRACT The urban gradient paradigm was used to investigate the influence of the urban environment on soils in Asheville, NC. A transect of forested plots was established from Asheville, NC to the Pisgah National Forest. The objectives of this study were to: (1) characterize the nature of the urban to rural land use gradient,(2) determine the response of soil physical and chemical properties to an urban environment, (3) characterize the response of the soil nematode community to an urban environment (as an indicator of the soil food web), and (4) determine if urban influences on the soil physical, chemical, and biological environment translate into measurable ecosystem effects. Soil chemical and physical properties were monitored along the gradient. Urban influences on the soil environment were observed. Urban soils were drier, had less organic matter content and were warmer than rural soils along the transect. The soil nematode community assemblage was observed along the gradient. Nematode diversity was not affected by the urban environment. However, the functional composition of the nematode community was influenced by the urban environment. Predatory and omnivorous nematodes were less abundant in the urban soils. Total nematode abundance was also lower in the urban soils. Maturity indices of the nematode community did not strongly reflect this change in the trophic composition of the community. Two ecosystem processes were monitored in this study, leaf litter decomposition and net nitrogen mineralization. The decomposition rate of a standard leaf litter (Quercus prinus) was slower in the urban plots, as evidenced by the ash-free dry mass remaining in the litter through time and the calculated rate constant. Net Nmineralization rates were greater in the urban soils. While litter decomposition rates were not correlated with soil environmental variables, rates of net N-mineralization were influenced by both the soil physical environment and the composition of the nematode community along the urban gradient. INDEX WORDS:

Urban ecology, Gradient, Soil chemistry, Nematodes, Maturity Index, Decomposition, N-mineralization

SOIL ECOLOGY ALONG AN URBAN TO RURAL GRADIENT IN THE SOUTHERN APPALACHIANS by MITCHELL A. PAVAO-ZUCKERMAN B.A., Binghamton University, 1995 M.S., University of Tennessee, 1998

A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree

DOCTOR OF PHILOSOPHY

ATHENS, GEORGIA 2003

© 2003 Mitchell A. Pavao-Zuckerman All Rights Reserved

SOIL ECOLOGY ALONG AN URBAN TO RURAL GRADIENT IN THE SOUTHERN APPALACHIANS

by

MITCHELL A. PAVAO-ZUCKERMAN

Electronic Version Approved: Maureen Grasso Dean of the Graduate School The University of Georgia August 2003

Major Professor:

David C. Coleman

Committee:

Miguel Cabrera Ted Gragson Paul Hendrix Carl Jordan

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DEDICATION For Mom and Dad, for always nurturing curiosity and For Jonas, Alex, Alison, Dennis, Elizabeth, Rebecca, and Oren, for reminding me why I thought Ecology was important

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ACKNOWLEDGMENTS The philosopher and deep ecologist Arne Naess argues that organisms are knots in a net of relationships, and that we can thus only be defined by our relationships with others. I’d like to thank the following for helping to shape my web of relationships in all stages of conducting this research. First and foremost, thanks to my advisor, Dave Coleman, for teaching me so much about soil ecology and how research is conducted (sensu lato), and for his guidance and enthusiastic motivation while conducting this research and writing the dissertation. I especially thank Dave for his understanding and support while I have tried to live in both Athens and Tucson over the past year. I thank my committee Miguel Cabrera, Ted Gragson, Paul Hendrix, and Carl Jordan for advice, insights, and comments throughout my time at UGA. Miguel and Paul made very helpful suggestions for statistics on my decomposition data. Ted’s comments helped me to think about how to place my work within the field of urban ecology. Special thanks to Carl for joining my committee late in the game so that I could defend in July. Thanks to Mark Hunter for serving as a committee member and his input in the design of this research. Thanks to the Coweeta LTER for financial and logistical support. Thanks to Linda Lee Enos for keeping things in the SEL running smoothly. Thanks to the Institute of Ecology for logistic support, and helping to send me around the country to talk about this research. Thanks also to Janice, Patsy, Thelma, and John.

vi To my office mates Stephanie and Breana - thanks for the venting (giving and getting), diversions, friendship, and competitive mound building. Thanks to those in the Soil Ecology Lab over the years, Christien, Shenglei, Sina, Hugo, and DAC for all sorts of discussions and diversions. Thank you to the land owners in Asheville for letting me use their properties in my study, which couldn’t have happened without your cooperation. Special thanks to Patrick Lance of the West North Carolina Nature Center. I would not know a Cephalobus from an Acrobleoides if it were not for the gracious hospitality of Howard Ferris, Mario Tenuta, and Inga Zasada, UC Davis. I especially thank Howard for teaching me how to work with the nematode weighted faunal analysis, and for answering questions I’ve had since my time in Davis; and Mario for putting in the most scope time with me (and for driving to Napa). Warning: roughly 250,000 nematodes were harmed in the production of this dissertation (actually death by formalin is a bit nastier than ‘harmed’). Thanks to Patricia Stock and the Department of Nematology, University of Arizona, for providing access to microscopes while visiting Barney over the past year. Extra special thanks to Geoff McCann for his hours grinding and weighing leaf samples. Thanks to Stephanie, Molly, and Tom in the Analytical Chemistry Lab for performing chemical analyses on my samples. The Research Services Chemical Analysis Laboratory, UGA, performed the heavy metal and base cation analyses. Thanks to Barrie Collins for his assistance with the GIS analysis of geographic data. J.P. also provided some GIS assistance (and good discussion).

vii Thanks to my friends and colleagues in the Institute and around Athens: Stuart, Mark, Steve, Cheryl, Erin, Mike, Misha, Josh, Cathy, Mike, Laura, Chris, Wyatt, and Keith; Cam, Anna, Steph, Sarah, Todd, Ramie, Tina, Doug, Jodie, Becky, John, and Josh. Thanks to the faculty of the Institute of Ecology and Environmental Ethics, especially Ron Pulliam, Laurie Fowler, Frank Golley, Bernie Patten, and Peter Hartel. Steve Holloway and Deb Martin, Geography, taught me a great deal about cities. Thanks to Richard Pouyat, USFS, and Margaret Carreiro, University of Louisville, for many discussions about urban soil ecology, and for sharing protocols. Long Live H.E. Kuchka! Dave, Eric, Suzanne, Rick, Felice, Becky, and Charles, its been a pleasure serving as ‘actual’ ecologist. Anyone who uses a comic book on comics as a text in class is ok in my book. Hey, hey, my, my - to the Malemen and the Stench of Monkeys Social Club - it’s better to burn out than it is to rust. Thanks to the ACS and the Master Chorale for letting me sing. Richard Andrus, Binghamton University, asked the first questions and provided the first experiences that lead me toward urban ecology. Thanks to my family (which has grown greatly since starting this research) and friends back up north. Your support, interest, and encouragement have helped me make my way though this. Brett and Larry, thanks for being the best siblings ever. Mom and Dad, thanks for everything you’ve done to get me to this point, your love, and enthusiastic encouragement.

viii To my wife, Barnet, keeper of the cats, and my partner in it all, I have been so lucky to have a partner with whom I can talk about all this, and who understands what I am going through. Thanks for the love, unwavering support, and for going first.

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TABLE OF CONTENTS ACKNOWLEDGMENTS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . v INTRODUCTION AND LITERATURE REVIEW . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 PHYSICAL, CHEMICAL AND BIOLOGICAL PROPERTIES OF URBAN SOILS IN ASHEVILLE, NC . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19 GENERIC DIVERSITY AND FUNCTIONAL COMPOSITION OF THE SOIL NEMATODE COMMUNITY ALONG AN URBAN TO RURAL GRADIENT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63 DECOMPOSITION OF CHESTNUT OAK (QUERCUS PRINUS) LEAVES AND NITROGEN MINERALIZATION IN AN URBAN ENVIRONMENT 100 GENERAL CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130 APPENDICES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 139 A. Study plot description . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 140

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INTRODUCTION AND LITERATURE REVIEW An Urbanized World We live in an increasingly human dominated world (Vitousek et al. 1997). United Nations data predict that the global urban population will grow from one-third of the total population in 1975 to two-thirds of the total population by 2025 (United Nations 1993). In the U.S., urbanization continues at a rapid rate. It is projected that the percentage of the U.S. population living in urban areas will increase from 74 % in 1986 to greater than 80 % in the year 2025 (Alig and Healy 1987). This trend toward an increasingly urban world underscores the need to understand the ecology of urban places. Historically, large scale, obvious, and direct effects of human activities have been incorporated into ecological studies (McDonnell and Pickett 1993). In the past decade, an increasing number of ecologists have criticized the manner in which the effects of humans are included in ecology, because ecologists have largely ignored many of the ecological manifestations of humans in basic ecology (McDonnell and Pickett 1993). Many ecologists call for the study of urban and suburban areas as ecosystems (Brown and Roughgarden 1989; Ludwig 1989). The addition of urban Long-term Ecological Research (LTER) sites (Baltimore and Phoenix) in 1997 suggests that studies of the ecology of urban areas are increasingly considered an important dimension of humanenvironment relationships.

2 Conceptual Approach Gradient Paradigm McDonnell and Pickett (1990) summarize the gradient concept as “the view that environmental variation is ordered in space, and that spatial environmental patterns govern the corresponding structure and function of ecological systems.” The gradient paradigm includes the concept of environmental gradients, as well as the analytical techniques which can be used to demonstrate and study it. Two types of gradients have been observed in nature, the simple and the complex. The simple gradient is an environmental series which uses only one measured environmental factor, while the complex gradient is a series based on several (possibly interacting) factors (Ter Braak and Prentice 1988). In addition to the two types of gradients, there are also two general classes of analytical techniques for use with gradients (Ter Braak and Prentice 1988). Direct gradient analysis is used when the environmental factors are ordered, such that, they can be represented by an unbroken, straight line across the landscape. Indirect gradient analysis is used when the underlying factors are not linearly ordered throughout the landscape, or are not initially clear. In such cases, ordination techniques are applied to the measurements of ecological parameters to define the underlying environmental gradient. McDonnell et al. (1993) state that urban-rural environmental gradients are complex and indirect, and can therefore be elucidated using indirect techniques.

3 Urban-Rural Gradients McDonnell and Pickett (1990) have suggested that the gradient paradigm is a powerful tool for examining urban influences on ecosystems due to the nature of urban geography. The ideal growth pattern for cities is a series of concentric rings of decreasing urbanization with distance from the urban core. Through an examination of the relationship between the environmental variation along a transect running from urban to rural land use areas, and the ecosystem structure and function on that transect, ecologists can define an urban-rural gradient (McDonnell et al. 1993). McDonnell and Pickett (1990) suggest that, due to the magnitude and types of ecological changes associated with urbanization, provides a variety of “unplanned experiments” and intense experimental manipulations, which can be utilized by ecologists for research, where rural sites can serve as a reference point for comparison with more urban stands (Pouyat et al. 1995). Pouyat (1991) extends this by stating that urban-rural gradients can provide “unplanned experiments” for pedological investigations of anthropogenic influences on soils. McDonnell and Pickett (1990) indicate that the anthropogenic manipulations along urban-rural gradients can be used to address basic ecological questions at a variety of spatial scales (i.e. hierarchy theory, disturbance theory, etc.), address questions which are specific to urbanization, and provide an unprecedented setting in which to integrate humans as subjects for ecological study. The utilization of the gradient paradigm in studies of urban areas therefore has implications for basic ecology and soil ecology, as well as quantifying the effects of urbanization.

4 The study of ecology along urban-rural gradients is relatively new; and, McDonnell and Picket (1990) suggest a framework to aid in the design of studies. This framework should account for: 1) factors constituting urbanization, 2) the effects of urbanization on biota and the environment, and 3) the resultant effects on ecosystems (McDonnell and Pickett 1990). Variation in geographical land-use characteristics (e.g. road density, population density) can be used to define urban-rural gradients. Urban landuse influences the physical and chemical aspects of the environment (e.g. elevated temperatures, heavy metal contamination). Conditions of the urban environment affect individual organisms as well as biotic communities. The physical, chemical, and biological influences of urbanization combine to produce ecosystem responses that can be quantified. A primary hypothesis of the gradient paradigm is that increasing levels of urbanization will have correspondingly stronger environmental and ecological impacts when compared to less developed sites. Urban Influences on Soils Urban Gradient Studies Several studies of urban ecology have implemented a gradient approach. Researchers find higher concentrations of heavy metals in forest soils located closest to the urban core, presumably due to urban pollution (Markkola et al. 1995; Pouyat and McDonnell 1991; Pouyat et al. 1995; Santas 1986). These studies also show a decreased microbial biomass and soil microbial activity (Markkola et al. 1995; Pouyat et al. 1995), as well as decreased nematode and microarthropod abundances (Pouyat et al. 1994) with increasing proximity to the urban core. These results are all correlated with soil metal

5 concentrations. Researchers on the New York City urban gradient study (URGE) also investigated the response of ecosystem processes to urban land use. They found that litter decomposition rates are higher in urban soils than rural soils, despite the effects of urban land use on the decomposer community (McDonnell et al. 1997). This process was driven by the presence of non-native earthworms in the urban plots, and a relative lack of any earthworms in rural plots (due to glacial defaunation), which stimulated decomposition and mineralization in their urban plots (McDonnell et al. 1997). New York, New York The New York urban-rural gradient transect was established in the late 1980's (McDonnell and Pickett 1990; McDonnell et al. 1993; White and McDonnell 1988). It extends from highly urbanized Bronx County, NY through suburban Westchester County, NY, to the rural Litchfield County, CT. In the New York gradient, study sites are on upland sites of similar soil series, oak-dominated overstory (except for White and McDonnell, 1988, who studied mixed hardwood-hemlock forests), of a minimum stand age of 60 years, and show no evidence of recent disturbance (Pouyat et al. 1995). Initial studies in the NY urban-rural gradient experiment (URGE) attempted to characterize the urban-rural environmental gradient. White and McDonnell (1988) compared nitrification and N mineralization potentials in mixed hardwood-hemlock forests in urban and rural areas. They report that the urban hemlock stand has significantly lower rates of net N mineralization and nitrification than the rural stand (White and McDonnell 1988). White and McDonnell (1988) suggest that high levels of

6 anthropogenic “urban grime” hydrocarbons may be limiting the activity of soil microbes and invertebrates in the more urban stands. Pouyat and McDonnell (1991) sampled three forest stands within each of three zones (urban, suburban, and rural) along the transect to characterize the gradient of heavy metal contaminant accumulation along the transect. These researchers found that forest floor concentrations of Cu, Ni, and Zn, and forest soil concentrations of Pb and Cu decreased significantly from urban to rural stands, and attributed this to high deposition rates in the more urban areas (Pouyat and McDonnell 1991). From the results of principal component analysis (PCA) of heavy metal concentrations in forest litter and soil, the authors suggest that total content values of heavy metals (floor + soil) provide a better estimate of the deposition gradient than either concentration alone (Pouyat and McDonnell 1991). Pouyat et al. (1995) used PCA to further characterize the urban-rural gradient in terms of soil chemical properties. They sampled each of the nine sites established by Pouyat and McDonnell (1991), and collected data on soil ion and metal components and soil physical properties. An important extension of the use of gradients in this study is the inclusion of geographic features associated with urbanization in characterizing the urban-rural gradient. So, not only did they order the gradient according to pH, heavy metal contamination, etc., Pouyat et al. (1995) also order the gradient in terms of traffic volume, road density, and population density. Pouyat et al. (1995) found heavy metal results similar to those reported by Pouyat and McDonnell (1991). There was a significant ordering of Pb, Cu, Ni, Ca, Mg, and K

7 along the urban-rural gradient, that was attributed to high rates of local deposition in the urban stands. For example, Cu and Pb showed a four-fold increase from rural to urban stands. While higher levels of soluble salt concentrations, pH, total N , and organic matter were found in the urban stands versus the rural stands, the authors did not report any significant variation among soil physical properties along the gradient (Pouyat et al. 1995). Geographical features were found to be highly correlated with variation among soil chemical properties along the transect, and those relating to car use (road density, traffic volume) most strongly predicted this variation (Pouyat et al. 1995). The proportion of urban land use adjacent to the sampling sites was also found to be significantly related to soil chemical properties. From these findings, the authors suggest that future studies of urban-rural gradients should incorporate more urban cover values to further evaluate the relationship between urban land use and soil chemical properties (Pouyat et al. 1995). These studies demonstrated that a gradient of urbanization exists in the New York City metropolitan area in terms of soil chemical properties, N cycling potentials, heavy metal accumulation, and geographical features. Other studies produced by the NY URGE relate this gradient of urbanization to soil faunal communities and related biogeochemical processes. Goldman et al. (1995) sampled 18 sites grouped according to degree of urbanization (based upon geographical features) into urban, rural, and suburban to determine if exposure to air pollution affects patterns of CH4 uptake, and to explore the links between N availability and CH4 uptake. From field measurements, CH4 consumption rates were found to be significantly higher in rural versus urban sites, and

8 soil NH4+ concentrations and total inorganic N levels were higher in rural than the urban sites (Goldman et al. 1995). The authors report that rates of CH4 consumption were positively correlated with soil NH4+ concentrations, and that this is in conflict with studies which have shown that CH4 consumption rates are decreased with N fertilization, citing studies which suggest that NH4+ can influence the activity of both nitrifiers and methanotrophs (Goldman et al. 1995). Pouyat et al. (1994) sampled three sites in each of three land use classifications (urban, suburban, and rural) to quantify the abundance of forest soil nematodes, microarthropods, and litter fungi, and to correlate the variation with these densities to forest soil chemical characteristics along the urban-rural gradient. The mean total and fluorescein diacetate (FDA)-active fungal lengths were highest in rural stands, and the effect of land use type on total fungal lengths was found to be significant (Pouyat et al. 1994). Fungal hyphal lengths and microarthropod densities were found to be negatively correlated with heavy metal contamination of the forest soils (Pouyat et al. 1994). Their findings indicate that contamination of forest soils in the New York Metropolitan area may be negatively impacting fungal, nematode, and microarthropod densities in forest soils. Pouyat et al. (1994) hypothesize that the observed patterns in population density of the soil fungivorous invertebrates may be in part a trophic response to lower fungal densities in the urban stands. Steinberg et al. (1997) sampled one of the three established plots in the urban, suburban, and rural stands, and conducted microcosm experiments on soil samples, to evaluate the effects of the gradient on earthworm abundances, and the effects of

9 earthworms on potential N mineralization and nitrification along the transect. Average earthworm density was found to be significantly higher in the urban plots than in the rural plots, and exotic species of earthworms were found in the urban soils (Steinberg et al. 1997). They demonstrated that earthworms have the potential to stimulate N mineralization along the gradient in that the presence of earthworms in urban soil microcosms lead to a switch from net N immobilization to net N mineralization (Steinberg et al. 1997). Steinberg et al. (1997) concluded that their findings indicate that elevated earthworm populations explain higher than expected nitrification rates in urban soils and play an important role in enhancing N cycling processes in urban soils. Oulu, Finland Principal component analysis has been used to produce the indirect SO2 and NOx pollution gradient around the city of Oulu, Finland (Ohtonen 1994; Ohtonen et al. 1992) (Markkola et al. 1995; Ohtonen and Markkola 1991). Twenty Scots pine sites were selected for the studies with the goal of using sites with the most homogeneous vegetational cover, that were same aged stands of Scots pine, and had humus pHs that did not vary between sites (Ohtonen and Markkola 1991). In a study along this urban pollution gradient, Ohtonen and Markkola (1991) studied the biological activity and amount of FDA active fungal mycelium in the mor humus of the ten most polluted (closest to the urban core) and the ten Scots pine sites furthest from the city. They found that while biological activity of fungi was lower in the more polluted sites, the length of FDA active fungal mycelium showed no significant variation amongst sites of varying pollution levels (Ohtonen and Markkola 1991).

10 Ohtonen et al. (1992) have examined the number of enchytraeids and nematodes in the mor humus layer of the Scots pine sites ordered on a gradient of humus layer sulfur levels. They have found that the number of enchytraeids and mycorrhizal fungi diversity decreased with increased mor humus sulfur and nitrogen concentrations, which occurred closer to the center of Oulu (Ohtonen et al. 1992). Ohtonen et al. (Ohtonen et al. 1992) hypothesize that the pollution affects the fungal population, and as mycorrhizae are food for enchytraeids, the enchytraeid population is affected by the quantity and quality of the mycorrhizae. These researchers did not find a correlation between nematode numbers and the pollution gradient (Ohtonen et al. 1992). Ohtonen (1994) reports the study of forest soil biology along a S and N concentration gradient around Oulu, Finland. Again, the 20 Scots pine sites are divided into the ten most and least polluted sites, which relates to distance from the core of pollution (Ohtonen 1994). Ohtonen (1994) found that microbial biomass C, N, and respiration rate decreased closer to the pollution core. In polluted soils there was a reduction in soil biomass, but a more intensive regeneration and intensified activity per biomass unit of microorganism was also reported (Ohtonen 1994). Ohtonen (1994) suggests that this indicates a shift in the microbial community toward a predominance of r-strategists under more polluted conditions, while K-strategists dominate under less polluted conditions. He concludes that these findings are in agreement with Odum’s theory of energetics in disturbed ecosystems (Odum 1985). Markkola et al. (1995) divide the 20 Scots pine sites of the Oulu pollution gradient amongst 4 pollution zones, based on proximity to the pollution source (urban

11 core), to examine fungal biomass along an urbanization gradient. They report that ectomycorrhizal reproductive biomass is seven times higher in the least polluted zone, while there is no significant difference between mycelial fungal mass between zones (Markkola et al. 1995). The fungal mantle of mycorrhizae is reported as having the lowest thickness in the most polluted zone (Markkola et al. 1995). Based upon a PCA of their data, Marrkola et al. (1995) suggest that total N, S, and Cu are the most important factors affecting fungal biomass. Washington, DC Santas (1986) tested his hypothesis that Pb disturbs the composition of soil communities by comparing communities along a gradient of urbanization (which he assumed was also a gradient of Pb pollution) in Washington, DC. The gradient was measured on a transect along Massachusetts Avenue, which runs in a constant direction from the center of the city to the suburbs. Using the US Capitol as the center, Santas (1986) created eight concentric circles (1.6, 3.2.......12.8 km in radii), and sampled the soil along the transect at one location per concentric circle. The soil was analyzed for Pb concentration, textural composition, percent organic matter, and percent moisture holding capacity. The Shannon-Weaver index of diversity (H´) for the soil community was calculated. Santas (1986) reports that sites located at greater distances from the center of the city had lower soil Pb concentrations and higher indices of species diversity than sites closer to the urban center. The association between diversity and stability is still disputed within ecology, but Santas’ (1986) results suggest that there is the potential for increased

12 stability in soil communities in less urbanized environments. Santas (1986) concludes that his data support the assumption that stressful conditions of lead, soil texture, moisture, and organic matter can be attributed to decreased diversity of soil communities. Brussels, Belgium Pizl and Josens (1995) report a study of earthworm communities along an urbanization gradient in the city of Brussels, Belgium. A transect was delineated along heavily trafficked streets running from the center of Brussels to the suburbs, and it was assumed that this was a decreasing gradient of urbanization (Pizl and Josens 1995). Soil and earthworm sampling was conducted at six public parks along the transect (Pizl and Josens 1995). Pizl and Josens (1995) found that while there is no relationship between earthworm community structure and the gradient of soil pollution, earthworm density increases from the center to the outskirts of Brussels. Earthworm biomass was negatively correlated with soil Pb, Cu, and Zn concentrations, and earthworm density was negatively correlated with soil Cd and Mg levels (Pizl and Josens 1995). The authors point out their data suggest that earthworms can be useful indicators of environmental pollution if the earthworm species and soil characteristics (such as, texture, water content, pH, etc.) are reported (Pizl and Josens 1995). The Study: an urban-rural gradient in the southern Appalachians Previous studies of urban ecology have focused on large, sometimes ‘primate’ (high rank in city size hierarchy) urban places (Baker et al. 2001; McDonnell et al. 1997; Pickett et al. 2001; Pouyat et al. 2002). I chose Asheville, NC as the city for this study in

13 part, because it is much smaller than most cities being studied by ecologists. As the field of urban ecology develops, it becomes important to include cities with different characteristics, because they can have differing environmental effects. For example, Brazel et al. (2000) found a relationship between city size and the magnitude of the urban heat island effect. Li et al. (2001) found that the concentration of heavy metals in Hong Kong soils is lower than that of some older cities in the United Kingdom. They attributed this to the relative age of the cities, and hence the duration of exposure to the environmental stress. Due to the difference in size of the urban places, it was expected that the nature and magnitude of urban environmental effects observed in this study would differ from that of other studies of urban gradients, in that environmental impacts of a smaller city would be of a lesser magnitude than those of a larger city (e.g., Pouyat et al. 1995; Pouyat et al. 1994). An urban-to-rural gradient transect was established, with Asheville, NC serving as the urban end of the transect. Twelve forested riparian zone plots were selected in the French Broad River Watershed. The plots are low elevation, have similar soil series, and have hardwood-conifer canopies. Four plots were established in each of 3 land use classes (urban, suburban, and rural). The main objectives of this study were to determine the nature of the soil response to a gradient of urban land use. Following McDonnell and Pickett (1990), and McDonnell et al. (1997), my more specific objectives were to:

14 (1) Characterize the urban to rural land use gradient, (2) Determine the response of soil physical and chemical properties to an urban environment, (3) Characterize the response of the soil nematode community to an urban environment (as an indicator of the soil food web), (4) Determine if urban influences on the soil physical, chemical, and biological environment translate into measurable ecosystem effects. I hypothesized that the urban soils would have: (1) lower soil water contents and higher temperatures, (2) decreased nematode diversity, and a reduction in nematode maturity indices, (3) faster rates of leaf litter decomposition and nitrogen mineralization

15 References Alig RJ, Healy RG (1987) Urban and built-up land area changes in the United States: an empirical investigation of determinants. Land Economics 63:215-226 Baker LA, Hope D, Xu Y, Edmonds J, Lauver L (2001) Nitrogen balance for the Central Arizona-Phoenix (CAP) ecosystem. Ecosystems 4:582-602 Brazel A, Selover N, Voes R (2000) The tale of two cities - Baltimore and Phoenix urban LTER sites. Climate Research 15:123-135 Brown JH, Roughgarden J (1989) US ecologists address global change. Trends in Ecology and Evolution 4:225-226 Goldman MB, Groffman PM, Pouyat RV, McDonnell MJ, Pickett STA (1995) CH4 uptake and N availability in forest soils along an urban to rural gradient. Soil Biology and Biochemistry 27:281-286 Li X, Poon C-s, Liu PS (2001) Heavy metal concentration of urban soils and street dusts in Hong Kong. Applied Geochemistry 16:1361-1368 Ludwig DF (1989) Anthropic ecosystems. Bulletin of the Ecological Society of America:12-14 Markkola AM, Ohtonen R, Tarvainen O, Ahonen-Jonnarth U (1995) Estimates of fungal biomass in Scots pine stands on an urban pollution gradient. New Phytologist 131:139-147 McDonnell MJ, Pickett STA (1990) Ecosystem structure and function along urban-rural gradients: an unexploited opportunity for ecology. Ecology 71:1232-1237

16 McDonnell MJ, Pickett STA (eds) (1993) Humans as components of ecosystems: subtle human effects and the ecology of populated areas. Springer-Verlag, New York McDonnell MJ et al. (1997) Ecosystem processes along an urban-to-rural gradient. Urban Ecosystems 1:21-36 McDonnell MJ, Pickett STA, Pouyat RV (1993) The application of the ecological gradient paradigm to the study of urban effects. In: McDonnell MJ, Pickett STA (eds) Humans as components of ecosystems: subtle human effects and the ecology of populated areas. Springer-Verlag, New York, pp 175-189 Odum EP (1985) Trends expected in stressed ecosystems. BioScience 35:419-422 Ohtonen A, Markkola AM (1991) Biological activity and amount of FDA mycelium in mor humus of Scots pine stands in relation to soil properties and degree of pollution. Biogeochemistry 13:1-26 Ohtonen R (1994) Accumulation of organic matter along a pollution gradient: application of Odum's theory of ecosystem energetics. Microbial Ecology 27:43-55 Ohtonen R, Ohtonen A, Luotonen H, Markkola AM (1992) Enchytraeid and nematode numbers in urban, polluted Scots pine (Pinus sylvestris) stands in relation to other soil biological parameters. Biology and Fertility of Soils 13:50-54 Pickett STA et al. (2001) Urban ecological systems: linking terrestrial ecological, physical, and socioeconomic components of metropolitan areas. Annual Review of Ecology and Systematics 32:127-157 Pizl V, Josens G (1995) Earthworm communities along a gradient of urbanization. Environmental Pollution 90:7-14

17 Pouyat RV (1991) The urban-rural gradient: an opportunity to better understand human impacts on forest soils. In: Society of American Forestry, Washington DC, pp 212-218 Pouyat RV, Groffman PM, Yesilonis I, Hernandez L (2002) Soil carbon pools and fluxes in urban ecosystems. Environmental Pollution 116:S107-S118 Pouyat RV, McDonnell MJ (1991) Heavy metal accumulations in forest soils along an urban-rural gradient in southeastern New York, USA. Water, Air, and Soil Pollution 57-58:797-807 Pouyat RV, McDonnell MJ, Pickett STA (1995) Soil characteristics of oak stands along an urban-rural land-use gradient. Journal of Environmental Quality 24:516-526 Pouyat RV, Parmelee RW, Carreiro MM (1994) Environmental effects of forest soilinvertebrate and fungal densities in oak stands along and urban-rural land use gradient. Pedobiologia 38:385-399 Santas P (1986) Soil communities along a gradient of urbanization. Revue d'Ecologie et de Biologie du Sol 23:367-380 Steinberg DA, Pouyat RV, Parmelee RW, Groffman PM (1997) Earthworm abundance and nitrogen mineralization rates along an urban-rural land use gradient. Soil Biology and Biochemistry 29:427-430 Ter Braak CJF, Prentice IC (1988) A theory of gradient analysis. Advances in Ecological Research 18:271-317 United Nations (1993) World Population Prospects. United Nations, New York

18 Vitousek P, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of earth's ecosystems. Science 277:494-499 White CS, McDonnell MJ (1988) Nitrogen cycling processes and soil characteristics in an urban versus rural forest. Biogeochemistry 5:243-262

19

PHYSICAL, CHEMICAL AND BIOLOGICAL PROPERTIES OF URBAN SOILS IN ASHEVILLE, NC1

1

Pavao-Zuckerman, M.A. and D.C. Coleman. To be submitted to Urban Ecosystems.

20 Abstract We implemented the urban gradient paradigm to investigate the response of the soil environment to urban land use in Asheville, NC. Soil physical and chemical properties along the land use gradient were analyzed. A principal components analysis of soil chemical properties indicated that the strongest response to urban land use was a decrease in soil organic matter, with base cations loading in the urban soils. Concentrations of some heavy metals were higher in the urban soils, however, the magnitude of difference was not very great. Monitoring of the soil environment through time indicated that urban soils are 1.1 E C warmer than the rural soils, and have lower soil moisture contents than rural soils. The results of this study indicated soil responses of a different nature and magnitude than reported in other investigations of soils along an urban to rural gradient. There is a great diversity in the geographic and demographic characteristics of cities, which should be used to guide a comparative approach to future investigations of urban soil environments. Keywords

gradient, soil chemistry, soil moisture, soil organic matter, southern Appalachians

21 Introduction Recently, ecologists have turned their attention to the long neglected and ignored urban ecosystems. This is in part due to the realization that many aspects of humanenvironment relations have not been included in basic ecological studies (McDonnell and Pickett 1990). Additionally there is a growing appreciation for the importance of urban places in the contexts of conservation (McKinney 2002; Miller and Hobbs 2002), environmental health (Mazari-Hiriart et al. 2000) and environmental ethics (Light 2001). One aspect of urban ecology that has received a good deal of attention is the study of urban soils (Beyer et al. 1995; Goldman et al. 1995; Groffman et al. 1995; Ohtonen et al. 1992; Pouyat et al. 1995; Zhu and Carreiro 1999). Soils are important because of their roles in nutrient cycling (Blair 1988; Coleman and Crossley 1996; de Ruiter et al. 1993), plant production (Setälä and Huhta 1991; Wardle 1999), and global nutrient budgets (Batjes 1998; Schimel and Gulledge 1998). Urban soils experience a wide array of environmental impacts. The urban heat island is an elevation in urban temperature relative to non-urban temperatures (McDonnell et al. 1993; Oke 1995), precipitation has been shown to increase in cities (Botkin and Beveridge 1997; Gilbert 1989), and urban hydrology is greatly modified (Paul and Meyer 2001). Deposition of pollutants, such as heavy metals, acid rain, and nitrogen species is common (Li et al. 2001; Lovett et al. 2000; Pouyat and McDonnell 1991). Researchers studying ecology along urban to rural gradients have found elevated levels of pollutants in urban soils (Ohtonen 1994; Ohtonen et al. 1992; Pouyat and McDonnell 1991; Pouyat et al. 1995). Such pollution gradients have been linked to shifts

22 in the abundance of soil organisms and the composition of soil organism communities (Pizl and Josens 1995; Pouyat et al. 1994; Santas 1986). Nutrient cycling in urban soils is also altered by these environmental impacts on urban soils (Carreiro et al. 1999; McDonnell et al. 1997; Pouyat et al. 1997). Most studies of soils in urban environments have been conducted in relatively large cities, such as New York City and Baltimore (Groffman and Crawford 2003; Pickett et al. 2001; Pouyat et al. 2002). The distribution of cities by size, however, shows that there are more small cities than large cities (Bessey 2002; Zipf 1949). It is likely that the nature and magnitude of environmental effects will differ between cities of different sizes. For example, Brazel et al.(2000) demonstrated a relationship between city size and the magnitude of the urban heat island effect. It is with this in mind that we chose Asheville, NC as the city in which to conduct this study, as Asheville has a population of around 70,000 (US Census 2000). This study was conducted to utilize the gradient paradigm to determine what the effects of an urban environment are on forest soil properties. McDonnell and Pickett (1990) have suggested that the gradient paradigm is a powerful tool for examining urban influences on ecosystems due to the nature of urban geography. Through an examination of the relationship between the environmental variation along a transect running from urban to rural land use areas, and the ecosystem structure and function on that transect, ecologists can define an urban-rural gradient (McDonnell et al. 1993). McDonnell and Pickett (1990) suggest that, due to the magnitude and types of ecological changes associated with urbanization, it provides a variety of “unplanned experiments” and

23 intense experimental manipulations, that can be used by ecologists for research. Rural sites along the gradient can serve as a reference point for comparison with more urban stands (Pouyat et al. 1995). A primary hypothesis of the gradient paradigm is that increasing levels of urbanization will have correspondingly stronger environmental and ecological impacts when compared to less developed sites. This study is reported in two parts, (1) an assessment of the nature of the urban gradient in and around Asheville, NC, and (2) monitoring several soil characteristics through time as a part of a larger study of the soil ecology in western NC (Pavao-Zuckerman 2003). Materials and Methods Site Description The study was conducted in and around Asheville, North Carolina, USA (35°35'N, 82°34'W). Field sites were selected along a 45-km transect running from Asheville to the Pisgah National Forest to the southwest (Figure 2.1). Four field sites were selected in each of three land-use classes: urban, suburban, and rural (classes defined by the political boundaries of Asheville and its suburbs). Each field site was located in the French Broad River watershed. Sites were selected to minimize the natural environmental variation between sites, and have low elevations (660-760 m), similar soils (Hapludults - mesic sandy loam), and characterized as hardwood-conifer canopies (see Appendix 1). Geographical Data Geographic data were compiled as a measure of the degree of urban land use at each field site. Population density was calculated for a 16 km2 area centered on each

24 field site from 1990 U.S. Census Bureau block level data in ARC View GIS software (ESRI Institute, Redlands, CA). Road density was calculated for a 16-km2 area centered on each field site from US Census Bureau Topologically Integrated Geographic Encoding and Referencing (TIGER) data in ARC View GIS Software. With both data sets, a 16km2 buffer was created around each digitized plot location. This buffer was intersected with the demographic and road coverages. Attributes (population and road density) in the resulting shapefile were summed to provide the geographic descriptor for each plot. Soil Physical and Chemical Analyses for Gradient Characterization Four 5 x 10 cm cores were collected at the field sites in the Spring of 2000. Bulk density was determined using four 5 x 10 cm cores per field site. Soil texture was determined using the hydrometer method (Elliott et al. 1999). Soil water content was determined seasonally by drying to constant weight at 105 °C. Subsamples were extracted using the Mehlich double acid procedure and analyzed for Cu, Ni, Mn, Co, Zn, Pb, Cr, and Cd (Mehlich 1953). Additionally, P, K, Ca, Mg, and Al were determined on the double acid soil extracts on a Thermo Jarrell-Ash 965 Inductively Coupled Argon Plasma (ICAP) analyzer. Soil pH was determined on a 2:1 water:soil slurry using a digital pH meter. Subsamples of soil were ground and analyzed for total C and N with a Carlo Erba, model 1500 total C/N analyzer (Milan, Italy). Total carbon and nitrogen were determined as the percent C and N on a dry weight basis. Soil organic matter content (percent) was determined by mass loss from combustion (450 EC for 4 hours).

25 Additional Soil Analyses To monitor soil variables as part of a larger ecosystem study, soils were sampled at each site once per season between March 2000 and October 2002. At each field site, four soil samples were taken to a depth of 10 cm, and then divided into 0-5 cm and 5-10 cm depths. Soil cores included the organic layer, but not the litter layer. Each sample consisted of four adjacent bulked soil cores (5 x 5 cm). Soil water content was determined seasonally by drying to constant weight at 105 ° C. Samples collected in the Spring of 2000, 2001, 2002 were used to obtain an annual estimate of soil C:N ratio and soil organic matter content. Subsamples of soil were ground to a fine powder and analyzed for total C and N with a Carlo Erba, model 1500 total C/N analyzer. Total carbon and nitrogen were determined as the percent C and N on a dry weight basis. Soil organic matter content (percent) was determined by mass loss from combustion (450 ° C for 4 hours). Soil temperature was measured using one HOBO (Onset Computer Corp.) data logger per site buried to a depth of 5 cm. Each logger took a simultaneous temperature reading to the nearest tenth of a degree every 4 hours. Mean daily temperatures were calculated for each field site. Soil microbial biomass was determined using the chloroform fumigation and extraction procedure (Vance et al. 1987). Samples were gently passed through a 2-mm sieve and fumigated for 48 hours. Samples were extracted with 0.5 M K2SO4 and filtered through #42 Whatman filter paper. Total organic carbon was determined on the extractants with a Shimadzu TOC-5000A Total Organic Carbon Analyzer. An extraction

26 coefficient correction factor of 0.38 was used in the calculation of microbial biomass C (Vance et al. 1987). Statistical Analyses All data were log-transformed to meet conditions of normality prior to statistical analysis. A Principal Components Analysis (PCA) was conducted on soil variables (heavy metals, nutrients, C:N ratio, total N, pH, organic matter) using the PC-ORD software package (McCune and Mefford 1999). Soil data were analyzed from the Spring 2000 sampling, and were analyzed for the total 0-10 cm samples. Data were relativized using general relativization prior to analysis in order for the data to be analyzed in the same scale (McCune and Mefford 1999). Soil chemical and physical properties were analyzed with a one-way ANOVA in S-Plus. Regressions between geographical features and distance to the urban core, and between PCA results and distance to the urban core were also conducted using S-Plus. A repeated measures ANOVA was used to analyze the soil moisture data using the MIXED procedure in SAS. Toeplitz was selected as the covariance structure according to Littell et al. (1998). The models generated least squares means that were analyzed using the pdiff option of the MIXED procedure. The pdiff option separated least square means using least significant difference. Results Gradient Characterization Geographical features showed clear trends along the gradient transect. A highly significant curvilinear relationship between population density and distance to the urban

27 core was found, with population density being higher closer to the urban core (R2 = 0.651, P