1 Assessment of Heavy Metal Contamination and Restoration Of

Home , Topsoil

Assessment of heavy metal contamination and restoration of soil food web

structural complexity in urban vacant lots in two post-industrial cities

Dissertation

Presented in Partial Fulfillment of the Requirements for the Degree Doctor of

Philosophy in the Graduate School of The Ohio State University

Kuhuk Sharma, M.Sc.

Graduate Program in Environmental Science Graduate Program

The Ohio State University

2014

Dissertation Committee:

Parwinder S. Grewal, Advisor

Larry Phelan, Co-Advisor

Nicholas T. Basta

Rafiq K. Islam

Kuhuk Sharma

2014

Abstract

Increasing proportions of vacant land parcels in post-industrial cities is a growing concern due to decreasing land value and increasing maintenance externalities. Utilizing this urban vacant land for growing food crops can promote local self-reliance and access to healthy food; specifically in low income disadvantaged neighborhoods. However, impact of heavy metal contaminants on soil quality, is a major concern for urban agriculture. Additionally, health of vacant lot soil also depends on the structural bio-diversity of the below ground soil food web.

Hence the specific objectives of this research were (i) to assess the level of soil heavy metal concentrations in two post-industrial cities and determine their potential human health risk (Chapter 2); (ii) to evaluate the relationship between heavy metal concentrations and the structure and function of the soil food web using nematodes as surrogates of soil microbial community (Chapter 3); (iii) to test a novel approach of transplantation of an intact soil core to reconstruct the structural complexity of a disturbed soil food web and restore its level of multi trophic interactions to a pre-disturbance level (Chapter 4) (iv) finally, to reconstruct the soil food web in urban vacant lot using intact soil cores from

ii relatively undisturbed forest soil, and assess the survival of the introduced nematode species under organic matter with different C:N ratios (Chapter 4)

We determined the extent of soil Pb, Cd, Zn, As and Cr concentrations in

43 vacant lots in two disadvantaged neighborhoods in Hough (Cleveland) and

Weinland Park (Columbus), Ohio. Results showed that compared to the

Ecological Soil Screening levels (Eco SSL) for human ingestion of soil, only 6% of the lots in Weinland Park and 53% in Hough neighborhood had Pb concentrations above the Eco SSL of 400 mg Pb/kg soil. Also, all the studied sites exceeded the Eco SSL value of 0.4 mg As/kg soil; however, soil As concentration in 94% of the lots in Weinland Park and 90% of the lots in Hough were not elevated beyond the natural background concentration in Franklin and Cuyahoga counties respectively. Associations with soil nematode community showed that the sensitive, higher trophic level omnivorous and predatory nematodes were found in low abundance indicating the disturbed nature of the urban soil food webs. Multiple regression analysis revealed a combination of As, Cd, Cr, soil texture and organic matter as significant variables whose interactions affected the abundance of nematodes and the community indices such as channel index, enrichment index and structure index. We observed distinct associations between metals, soil properties and nematode parameters in the two neighborhoods.

All the studied vacant lots were not contaminated and metal concentration was not uniform across a given lot. To restore soil food web complexity in lots with little or no metal contamination, we tested a new approach of intact soil core

iii transplantation and hypothesized that the missing nematode trophic guilds (along with associated soil organisms) can be reestablished using intact soil cores (9cm dia, 10cm deep) brought carefully from undisturbed forest. Laboratory and field analysis showed that higher trophic level nematodes can spread out of the transplanted cores and colonize a 2.25 m2 area within 2 weeks, with >50% increase in structure index within 3 weeks.

Further analysis was carried out in vacant lots with metal concentrations lower than the USEPA established Soil Screening Levels (SSL). We tested the potential of organic amendments differing in their C:N ratios such as compost, peat and grass clippings to help in sustenance of the introduced nematode trophic guilds. Results showed that the use of organic compost and grass clippings as soil amendments supported maximum increase in abundance of higher trophic level nematodes and improvement of nematode community structure and maturity indices. Results from this study can help improve soil health in urban vacant lots, thus eliminating the need for large-scale topsoil replacements. This will pave the way for establishment of sustainable and safe urban food production systems.

Acknowledgements

I would like to thank my committee members Dr. Parwinder Grewal, Dr.

Larry Phelan, Dr. Nick Basta and Dr. Rafiq Islam for all of their guidance and support over the last few years. Their constant motivation and encouragement was an important factor in helping me through to the end of my research. I thank

Dr. Grewal for seeing the potential in me and accepting me to be a part of his team. His zeal and energy pushed me through the difficult moments and his mantra of positive encouragement guided me as I went over the completion of this thesis. I look up to you Dr. Grewal and your approach in facing challenges is something that I would also like to develop as I face the rest of my endeavors.

I am also thankful to the all of my lab members for their help and support during my research. I thank Dr. Zhiqiang Cheng for working with me and assisting me with sampling, data collection, experimental designs and help with statistical analyses. I also thank Dr. Ruisheng An and Amr Badawy for making several trips with me to the forest sites and their invaluable help with the physically strenuous field work. I am also grateful to Dr. Harit Bal for providing guidance and help from even before I officially came to the Ohio State University, and being a good host, lab member and friend ever since. I thank Dr. Priyanka

Yadav for all the help she provided in my field work and the constant source of v guidance during my Teaching Assistantship, course work and during my stay in

Columbus.

I am also thankful to the administrative staff of the Environmental Science

Graduate Program, especially Dr. Richard Moore for lending a listening ear whenever required. I thank Maurea Al-Khouri and Sarah Straley for all their administrative support. I am thankful to the staff and faculty in the Department of

Entomology for always being ready to help me with any request and never letting there be a dull moment. I thank my fellow graduate students, alumni from the department and all of my friends in Wooster and Columbus.

I am thankful to my family for their whole hearted support in all my undertakings, always pushing me to achieve more and making me the confident and independent person I am today. I want to especially thank my pillar of strength, Pranay Jain. Thank you for bearing with me through my meltdowns and rejoicing my accomplishments. I could not have completed this journey without you or without my irreplaceable friends for life, Aparna Lakshmanan, Aditi

Sengupta and Kshipra Chandrashekhar. Thank you for making my life so much more fun.

Vita

2006...... B.S. Life Sciences, University of Mumbai

2008...... M.S. Life Sciences (Biotechnology),

University of Mumbai

2009 to 2010 ...... Fay Fellow, Environmental Science

Graduate Program, the Ohio State

University

2010 to 2011 ...... Graduate Teaching Associate, School of

Environmental Science and Natural

Resource, the Ohio State University

2011 to 2012 ...... Graduate Teaching Associate, Center for

Life Sciences Education, the Ohio State

University

2012 to 2014 ...... Graduate Research Associate, the Ohio State

University

Publications

Sharma, K., Basta, N. T., Grewal, P.S. Soil heavy metal contamination in residential neighborhoods in post-industrial cities and its potential human exposure risk. (in press) 2014. Urban Ecosystems vii

Field of Study

Major Field: Environmental Science/Ecology

viii

Table of Contents

Abstract ...... ii Acknowledgments...... v Vita ...... vii Table of Contents ...... ix List of Tables ...... xi List of Figures ...... xiii Chapter 1 Introduction ...... 1 References ...... 11 Chapter 2 Soil heavy metal contamination in residential neighborhoods in post- industrial cities and its potential human exposure risk ...... 15 Abstract ...... 15 Introduction ...... 17 Materials and Methods ...... 20 Results ...... 27 Discussion ...... 42 Acknowledgements ...... 50 References ...... 51 Chapter 3 Relationship between heavy metal contamination and soil food web health in vacant lots slated for urban agriculture in two post-industrial cities ...... 57 Abstract ...... 57 Introduction ...... 58 Materials and Methods ...... 61 Results ...... 64 Discussion ...... 77 Acknowledgements ...... 94 References ...... 95 Chapter 4 A novel approach to restoring structural complexity in soil food webs...... 100

Abstract ...... 100 Introduction ...... 102 Materials and Methods ...... 106 Results ...... 114 Discussion ...... 143 Acknowledgements ...... 154 References ...... 155 Chapter 5 Overall Discussion and Conclusions ...... 161 References ...... 173 Literature Cited ...... 177

List of Tables

Table 2.1 Mean, median, minimum, maximum, 25th and 75th percentile of the measured heavy metals - arsenic (As), cadmium (Cd), chromium (Cr), lead (Pb) and zinc (Zn); and soil parameters – soil texture including % sand, % silt and % clay, soil pH, % soil moisture, % organic matter and active carbon (mg/kg) content, in the Hough (Cleveland, Ohio) and Weinland Park (WP) (Columbus, Ohio) neighborhoods...... 30

Table 2.2 Mean background concentrations (mg/kg) of the studied heavy metals in the state of Ohio and the US, along with the observed means in the two neighborhoods in Cleveland and Columbus. Mean concentrations observed along a freeway passing through a rural area around Wooster are also presented for comparison ...... 33

Table 2.3 Average regulatory guidance values for metals (mg/kg) in residential soil of 30 US states including Ohio, along with the values set by the USEPA (Peterson et al., 2006); and the USEPA generic soil screening levels (SSLs) for human ingestion of soil (mg/kg) (USEPA 1996)...... 36

Table 3.1 Mean, Standard Error (SE) of mean and the Range for soil physical, chemical and biological properties in vacant lots in the Weinland Park (Columbus, Ohio) and Hough (Cleveland, Ohio) neighborhoods.………………………………...... 65

Table 3.2 List of nematode genera identified and their assigned colonizer-persister scale values (numbers in parenthesis, following Bongers 1990) from soil samples collected from vacant lots in the Hough (Cleveland, Ohio) and Weinland Park (Columbus, Ohio) neighborhoods ...... 67

Table 3.3 Significant predictor variables and their respective degrees of freedom (df), F value, P value (at α ≤ 0.05), the adjusted R squared value for the model, and the direction of regression slope for the individual variables obtained by multiple regression analysis with all heavy metal and soil physical and chemical properties on different nematode community parameters in the Weinland Park neighborhood, Columbus, Ohio…………73

Table 3.4 Significant predictor variables and their respective degrees of freedom (df), F value, P value (at α ≤ 0.05), the adjusted R squared value for the model, and the direction of regression slope for the individual variables obtained by multiple regression analysis with heavy metal and soil physical and chemical properties on different nematode community parameters in the Hough neighborhood, Cleveland, Ohio……..…………...78 xi

Table 4.1 Mean abundance and standard error of mean (SEM) for total numbers of nematodes and genera and nematode genera belonging to different trophic groups along with the calculated community indices from soil samples (10 g each) collected from GrossJean forest woodlot and the turfgrass plots in Wooster, Ohio...... 118

Table 4.2 Mean abundance and standard error of mean (SEM) for total numbers of nematodes and genera, and nematode genera belonging to different trophic groups along with the calculated community indices from soil samples (10 g each) collected from Waterman farm woodlot and the vacant lots in Weinland Park neighborhood in Columbus, Ohio ………………………………...... 128

Table 4.3 Mean and standard error of mean (SEM) of percent abundance of nematodes classified according to (i) different feeding types, PPN: plant parasitic, BF: Bacteria feeding, FF: Fungus feeding, PR: Predatory and OM: Omnivorous nematodes; (ii) colonizer-persister (C-p) scale, (iii) the ratio of bacterivores to total opportunistic nematodes and (iv) calculated nematode community indices, EI: enrichment index, SI: structure index, CI: channel index, MI: maturity index, PPI: plant parasitic index, and CMI: combined maturity index; for Oct 2013 (week 11 of the study) in vacant lots in Weinland Park neighborhood in Columbus, Ohio, under different treatments………………………..……………………………………………………..141

xii

List of Figures

Figure 2.1 Urban vacant lots in the Hough neighborhood in Cleveland, and the Weinland Park neighborhood in Columbus, Ohio……………………………………………….. 22

Figure 2.2 Mean (+ SE) for soil characteristics measured in selected vacant lots in Weinland Park (Columbus) and Hough neighborhoods (Cleveland), Ohio. Means (bars) with different letters are significantly different (Tukey’s mean comparison) at P < 0.05...... 28

Figure 2.3 Mean (+ SE) concentrations of heavy metals measured in selected vacant lots in Weinland Park (Columbus) and Hough neighborhoods (Cleveland), Ohio. Means (bars) with different letters differ significantly (Tukey’s mean comparison) at P < 0.05...... 32

Figure 2.4 Principal component analysis loading plot for the 1st and 2nd component axis for heavy metal concentrations and soil physical and chemical parameters in the Hough neighborhood in Cleveland, Ohio. M = % soil moisture and OM = % organic matter…………...... ……37

Figure 2.5 Principal component analysis loading plot for the 1st and 2nd component axis for heavy metal concentrations and soil physical and chemical parameters in Weinland Park neighborhood in Columbus, Ohio. OM = % organic matter...... 40

Figure 3.1 Mean (± S.E.) total number of nematodes (per 10g soil) categorized by the colonizer-persister (c-p) scale 1 to 5 (Upper) and by their feeding types – plant parasitic (PPN), bacteria feeding (BF), fungus feeding (FF), omnivores (OM) and predatory nematodes (PR) (Lower) in the Weinland Park neighborhood, Columbus and Hough neighborhood, Cleveland (Ohio, USA). Asterisks on the pair of bars indicate significant differences between the neighborhoods at P ≤ 05………………………………...... 68

xiii neighborhoods (Ohio, USA). Data presented are Mean (± SEM), asterisks on the pair of bars indicate significant differences between the two neighborhoods at P ≤ 0.05 ...... 69

Figure 3.3 Principal component analysis of the environmental variables (As, Cd, Cr, Pb, Zn, % clay, % sand, % silt, pH, moisture, organic matter and active C content) and nematode counts and indices in the Weinland Park neighborhood (Columbus, Ohio). Nematode variables have been divided based on their colonizer –persister scale (c-p) scale 1 to 5 (3.4 a), their feeding groups: bacteria feeding (BF), fungus feeding (FF), omnivores (OM), predatory (PR) and plant parasitic nematodes (PPN) (3.4 b) and the various nematode indices: enrichment index (EI), structure index (SI), maturity index (MI), plant parasitic index (PPI), channel index (CI), ratio of free living to plant parasitic nematodes (FLN/PPN), Shannon's diversity index, Menhinic's richness index, and evenness index (3.4 c)………………………………………………………………….71

Figure 3.4 Regression slopes for the lower trophic level bacteria and fungus feeding nematodes versus As, Cd, Cr, Pb and Zn conentrations (mg/kg soil) in Weinland Park neighborhood in Columbus, Ohio………………………………………………………74

Figure 3.5 Principal component analysis of the environmental variables (As, Cd, Cr, Pb, Zn, % clay, % sand, % silt, pH, moisture, organic matter and active C content) and nematode counts and indices in the Hough neighborhood (Cleveland, Ohio). Nematode variables have been divided based on their colonizer –persister (c-p) scale 1 to 5 (3.5 a), their feeding groups: bacteria feeding (BF), fungus feeding (FF), omnivores (OM), predatory (PR) and plant parasitic nematodes (PPN) (3.5 b) and the various nematode indices: enrichment index (EI), structure index (SI), maturity index (MI), plant parasitic index (PPI), channel index (CI), ratio of free living to plant parasitic nematodes (FLN/PPN), Shannon's diversity index, Menhinic's richness index, and evenness index (3.5 c)...... 76

Figure 3.6 Regression slopes for the lower trophic level bacteria and fungus feeding nematodes versus As, Cd, Cr, Pb and Zn conentrations (mg/kg soil) in Hough neighborhood, Cleveland,Ohio…………………………………………………………..80

Figure 3.7 Regression slopes for Eudorylaimus versus As, Cd, Cr, Pb and Zn conentrations (mg/kg soil) in Weinland Park (Columbus, Ohio) and Hough (Cleveland, Ohio) neighborhoods ……………………………………………………………………71

Figure 4.1 Mean (± S.E.) total abundance and abundance of bacteria feeding, fungus feeding, plant parasitic, omnivorous and predatory nematodes in frames with the transplanted forest soil cores at 5, 10, 15 and 20 cm distances from the edge of the core, across the time period of 5 weeks. Letters over bars indicate significant difference between distances in individual week at P ≤ 0.05……………………………………..115

Figure 4.2 Mean (± S.E.) total abundance and abundance of bacteria feeding, fungus feeding, plant parasitic, omnivorous and predatory nematodes (extracted from 10g soil) in xiv turf-grass plots with transplanted forest soil core and plots with commercially available, greenhouse heated topsoil spread on the surface, across a time period of 8 weeks. Letters over bars indicate significant difference significant differences in the treatments in individual week at P ≤ 0.05……………………………………………………………120

Figure 4.3 Mean (± S.E.) values for abundance of bacteria feeding, fungus feeding, plant parasitic, omnivorous and predatory nematodes in turf-grass plots with transplanted core and plots with commercially available, greenhouse heated topsoil spread on the surface, at 15, 30 and 45cm distances across a time period of 8 weeks. Letters over bars indicate significant difference between the two treatments in that individual week at P ≤ 0.05……………………………………………………………………………………122

Figure 4.4 Mean (± S.E.) values for enrichment index, structure index, channel index, maturity index, plant parasitic index and combined maturity index in turf-grass plots with transplanted core and plots with commercially available, greenhouse heated topsoil spread on the surface, across a time period of 8 weeks. Letters over bars indicate significant difference between the two treatments in individual weeks at P ≤ 0.05…………………………………………………………………………………….126

Figure 4.5 Means +SEM (standard error of mean) of total nematode abundance and abundance of different feeding types: bacteria feeding, fungus feeding, plant parasitic, omnivorous and predatory nematodes (per 10g soil), in the two vacant lots in Weinland Park, Columbus, Ohio, over a time period of 11 weeks after forest soil core transplantation, under different organic amendments. Letters on top of the bars indicate significant differences between the treatments within each week P≤0.05 … … … … 134

Figure 4.6 Means +SEM (standard error of mean) of calculated nematode community indices including enrichment index, structure index, maturity index and plant parasitic index, in the wo vacant lots in Weinland Park, Columbus, Ohio, over a time period of 11 weeks after forest soil core transplantation under different organic amendments. Letters on top of the bars indicate significant differences between the 3 organic amendments within each week at P≤0.05 ...... 137

Figure 4.7 Mean +SEM (standard error of mean) of spread and abundance of higher trophic level omnivorous nematodes at 15, 30 and 45cm distances around the transplanted forest soil core, in the vacant lots in Weinland Park neighborhood in Columbus, Ohio, under different organic amendments. Graphs (A) represents only core with no organic amendment, (B): core + compost, (C): core + grass and (D): core + peat amendment. Letters on bars indicate significant differences between the distances in each week at P≤0.05...... 139

Figure 4.8 Mean +SEM (standard error of mean) of spread and abundance of higher trophic level predatory nematodes at 15, 30 and 45cm distances around the transplanted forest soil core, in the vacant lots in Weinland Park neighborhood in Columbus, Ohio, under different organic amendments. Graphs (A) represents only core with no organic xv amendment, (B): core + compost, (C): core + grass and (D): core + peat amendment. Letters on bars indicate significant differences between the distances in each week at P≤0.05 ...... 140

Figure 4.9 Temporal dynamics of the nematode food web in vacant lots in the Weinland Park neighborhood in Columbus, Ohio, from August 2013 to October 2013, before and after transplantation with an intact forest soil core, with different organic soil amendments applied in August 2013...... 142

xvi

Chapter 1: Introduction

The term “vacant land” is associated with negative connotations which generate images of empty spaces with overgrown weeds and shrubbery or boarded up, old buildings (Bowman and Pagano, 2004). The abandoned buildings are generally old homes, industries and stores that were shut down mostly due to the recent economic crisis and home foreclosures. As a result, the increasing unemployment forced people to move out in search of new job opportunities

(Bowman and Pagano, 2004; Goldstein et al., 2001; Adams et al., 1993). The city, which has to bear the expense of demolition of these dilapidated structures, also incurs other maintenance costs such as regular mowing of the property, fencing and removing trash. Additionally, such areas of neglect face an increase in criminal activities such as drug peddling and are often encroached upon by the homeless and poor (Goldstein et al., 2001; Accordino and Johnson 2000; Spelman

1993). This further strengthens the association of vacant land with negative adjectives such as unsafe or dangerous (Bowman and Pagano, 2004).

The significant increase in the proportion of vacant lots in post-industrial cities such as Cleveland (OH), Baltimore (MD) and Detroit (MI) (Schilling and

Logan 2008), has been a constant source of concern for City Planning and

Economic Development Divisions. Although there is no official estimate of the scale of vacant property in US, numbers provided by different studies are dismal.

Reports estimate the presence of approximately 18,000 vacant parcels in the city of Cleveland, Ohio (Cuyahoga County, Food Policy Coalition, 2010) and 8,300 parcels within Boston city limits (Goldstein et al., 2001). Even the highly urbanized city of New York (NY) has almost 4,200 acres of vacant land within

Staten Island, close to 2,500 acres in Queens and almost 1,200 acres in the

Brooklyn area (NYC Department of City planning, 2010). Bowman and Pagano

(2004), report a larger abundance of vacant land within cities in southern US as opposed to the cities in northeast or western US.

This large mass of underutilized land has the potential to provide essential ecosystem services including food security, especially in low income, disadvantaged neighborhoods. Such neighborhoods gradually turn into food desserts due to increasing distances from food markets, since the location of such a store may be governed by the spending power and population density of the surrounding area (Larsen and Gililand, 2008). Some disadvantaged neighborhoods in post-industrial Midwestern US cities like Cleveland and Detroit do not have the spending power or the population density to support large grocery stores that sell healthy food items. This makes it difficult for lower income families that do not have easy access to a car, to make regular trips to such stores for healthy food supplies (Larsen and Gililand, 2008; Zenk et al., 2005).

Urban agriculture may hold the key to allow economically disadvantaged neighborhoods in post-industrial cities to become self-reliant in locally produced, fresh fruits and vegetables, and also provide economic relief by creating employment opportunities (Grewal and Grewal 2012; Adams et al. 1993).

Therefore, the first component of my research was to assess the viability of vacant lots in disadvantaged neighborhoods in 2 post-industrial cities of

Cleveland and Columbus, Ohio, as community based food production systems.

Studies have predicted the ability of cities like Cleveland to generate up to 100% of their fresh produce requirement using vacant land and roof top space available within the city boundary (Grewal and Grewal 2012). With several additional benefits derived out of community gardening such as a recreational and social gathering opportunity, social cohesion, improved human physical and psychological well-being, reduction in crime and noise, improved aesthetic appeal of the community, increase in value of adjacent land, an opportunity to provide nutritional and environmental education to young and old, employment opportunities; along with a host of ecological services such as regulation of temperature, air and water pollution , storm water absorption, carbon absorption, increased biodiversity and biological control of pests (Patel, 1991; Ferris et al.,

2001; Wakefield et al., 2007; Blaine et al., 2010; Yadav et al., 2012); the pull towards urban agriculture has been persuasive.

However, there are concerns about soil quality and contamination in urban areas. Craul (1992) defined urban soil as a “man-made, non-agricultural layer,

50cm thick, produced by mixing, filing or contamination of land surface in urban or sub-urban areas”. It does not have any characteristic soil profile consisting of specific horizons due to excavation, stockpiling and mixing. Urban soil has a heterogeneous composition vertically as well as horizontally that is strongly influenced by human activities. Its mineralogical profile and metal composition may be primarily determined by the local bedrock geochemistry (Adriano 2001;

Kabata-Pendias 2000), if it has not been excavated and replaced. However, it may also have a lot of foreign substances such as brick, stones, wood, plastic and construction debris; and may be contaminated with heavy metals and various hydrocarbons originating from point and non-point sources (Jim, 1998; Craul,

1992). The soil does not have any structure and may be highly compacted as a result of heavy foot-traffic, machinery or construction activities.

Contamination with heavy metals is one of the main risks in utilizing urban vacant lots for recreational activities or for growing food (Guo et al. 2006;

McClintock 2012). High soil concentrations of Pb, As, Cd, Cr and Zn are remnants of past land use and industrial histories of the cities (Mielke et al., 1999,

2000). Significantly high Pb concentrations can be attributed to contaminant particles in air originating from leaded gasoline use in the 1960s which settled onto the soil. Another major factor could be Pb dust originating from scraping off the leaded paint from walls of old houses (Mielke et al., 2001) during demolition.

Cd and Zn may also be found as contaminants in the leaded paint as well as being present in vehicle exhaust fumes that settle on the soil. Hence it is the top layer of

4 soil (0 to10~15 cm) that usually has the maximum accumulation of metals (Guo et al., 2006; Turer et al., 2001; Jim 1998) and this prevents the usage of urban vacant lots as potential food gardens. Additionally, metals based on their concentration in soil and bioavailability, may be taken up by bacteria (Zouboulis et al., 2004) or plants such as food crops, hence entering the food chain.

Sustainable urban agriculture requires healthy soil with a well- established, complex soil food web; to provide essential ecosystem services such as bio-control of pests and pathogens, effective nutrient mineralization, organic matter decomposition, carbon sequestration, and degradation of organic contaminants (Yadav et al., 2012; Brussaard et at., 2007; Ferris and Matute,

2003). Urban soil has interrupted nutrient cycling and altered floral and faunal compositions (Pavao-Zuckerman and Coleman, 2007; Jim, 1998; Craul, 1992;

Park et al., 2010) and often a lack of higher trophic levels in the soil food web as compared to relatively undisturbed forest soil (Bongers and Ferris, 1999).

Ecosystems with such degraded/disturbed soils also have decreased resilience and are more susceptible to damage caused by a second disturbance (Hedlund et al.,

2004). Absence of a mature soil food web and healthy soil requires addition of large amounts of fertilizers, pesticides, weedicides and other synthetic chemicals, which can further deteriorate soil quality and increase concentration of metals in soil. Additionally, heavy metal contamination of soil may negatively impact organic matter decomposition thereby inhibiting efficient nutrient cycling

(Zouboulis et al., 2004).

Restoring the soil food web complexity and bringing back the missing trophic guilds can help improve the functioning of an urban ecosystem (Brussards et al., 2007; Duffy et al., 2007; Hedlund et al., 2004) and concomitantly advance food growing systems. Changes in the diversity of the higher trophic levels

(omnivores and predators) can significantly impact producer (plant) biomass

(Duffy et al., 2007; Borer et al., 2005). Borer et al. (2005) showed that presence of predators in the food chain helped increased plant biomass to a larger extent than application of fertilizers in the absence of predators. Hence, the second component of my research was to try and re-construct the structural complexity of the soil food web in urban vacant lots to support urban agriculture.

Management practices followed in urban gardening include use of organic amendments such as compost, mulch and mixed cropping to supply the soil with

C, N, P and additional nutrients; along with the use of chemical fertilizers and pesticides. Fertilization may increase soil nutrients and cation exchange capacity

(CEC), and also improve soil texture, aggregate formation, porosity and moisture retention. However, these are not sufficient to restore higher trophic levels in the soil food web (Borer et al., 2005) and improve its resilience, nutrient cycling capacity or bio-control potential. I hypothesized that the missing trophic guilds in the urban soil food web can be re-established to bring back the functional complexity of the soil food web.

My specific objectives were to (i) assess the level of As, Cd, Cr, Pb and

Zn soil contamination in two disadvantaged residential neighborhoods, Hough

6 neighborhood in Cleveland and Weinland Park neighborhood in Columbus, Ohio; and to determine the potential human health risk of these contaminants (Chapter

2); (ii) evaluate the relationship between heavy metal concentrations and the structure and function of the soil food web in the urban vacant lots (Chapter 3);

(iii) test a novel approach of transplantation of intact soil cores, brought in form an undisturbed forest area, to reconstruct the structural complexity of a disturbed soil food web and restore its level of multi trophic interactions to a pre- disturbance level (Chapter 4) (iv) and finally, to reconstruct the soil food web in urban vacant lots in the disadvantaged residential neighborhoods, using intact soil cores from relatively undisturbed nearby forest soil, and assess the survival of the introduced higher trophic levels under organic matter with different C:N ratios

(Chapter 4).

I made use of the soil nematode community as a representative of the structure and complexity of the below ground soil food web. Nematodes are important components of the soil ecosystem and play an essential role in energy transfer, nutrient transformation and organic matter decomposition (Chen et al.,

2009; Ferris et al., 2001). More importantly, they serve as efficient bio-indicators of soil food web health due to their presence at multiple trophic levels of the food web, from primary consumers that feed on plant, to decomposers feeding on bacteria and fungi, to tertiary level consumers such as omnivorous and predatory nematodes (Shao et al., 2008; Coleman et al., 2004; Ferris et al., 2001; Yeates and

Bongers, 1999). Additionally, different nematode genera have different

7 sensitivities to metal contaminants (Ekschmitt and Korthals 2006). They are well adapted to a wide range of environmental conditions and respond rapidly to any change or disturbance around them. Other features such as their size, abundance, presence in all soil types, short life cycle and visible internal anatomy (Shao et al.,

2008; Ferris and Bongers, 2006) also make nematodes useful bio-indicators.

Results from my research showed that all of the urban vacant lots in the residential neighborhoods of Hough in Cleveland and Weinland Park in

Columbus, Ohio, were not contaminated. Only a few lots (less than 10%) had soil

As concentration higher than the natural background levels in Cuyahoga and

Franklin counties. Additionally, only 6% of the lots in Weinland Park and 53% in

Hough had soil Pb concentrations higher than the USEPA established Soil

Screening Level (Eco SSL) for Pb; while none of the lots exceeded the SSL for

Zn. Also sample analysis from different sections of the lots showed that they were not uniformly contaminated across the entire soil surface. Hence some of these vacant land parcels could definitely be repurposed as future food gardens.

Also there was a high correlation between the soil physical and chemical properties and heavy metal concentrations suggesting strong interactions between these environmental factors when influencing the health of the soil food web.

A comprehensive nematode community analysis of the vacant lots showed that the soil food web is lacking structural complexity and does not have a high abundance of the higher trophic guilds. Correlations between the soil nematode community and the physical and chemical properties and heavy metal

8 concentrations showed that in the absence of the higher trophic level omnivorous and predatory nematodes, the opportunistic bacteria and fungus feeding nematodes could serve as indicator of heavy metal stress. Fungus feeding nematodes in the Weinland Park neighborhood showed strong negative correlations with soil Cd, Zn and % sand. In the Hough neighborhood, overall soil texture, organic matter and soil Cr and As concentrations were significantly correlated with the abundance of lower trophic level bacteria and fungus feeding nematodes.

Our novel approach of restoring soil food web complexity via intact core transplantation showed encouraging results. These cores brought in from relatively undisturbed forest soil have high functional diversity with the presence of multiple trophic levels that can fill in the vacant niches within the nutrient rich soil ecosystems in vacant lots. Nematodes were able to move out of the transplanted core and colonize surrounding soil in large numbers in the lab and field trials and resulted in significant improvements in the nematode community structure and maturity indices. When analyzed in conjunction with organic amendments differing in their C:N ratios, organic compost with a lower C:N ratio of 12:1 proved to be the most optimum amendment to bring about the maximum improvement in the functional complexity of the urban soil food webs.

Results from this research have significant implications for economically disadvantaged neighborhoods in encouraging the use of vacant lots as ideal venues for urban agriculture and promoting the community’s self-reliance in

9 production of fresh fruits and vegetables. This study also brings to the forefront a fast, inexpensive and ecological sound method of restoring biodiversity and health of soil food webs to regain the full spectrum of potential ecosystem services from vacant patches of land.

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Chapter 2: Soil heavy metal contamination in residential neighborhoods in

post-industrial cities and its potential human risk

Abstract

This study assessed the extent of potential human risk to heavy metal exposure by comparing concentrations of arsenic (As), cadmium (Cd), chromium (Cr), lead

(Pb) and zinc (Zn) in soil in 43 vacant lots in two low income neighborhoods,

Hough (Cleveland, Cuyahoga County, Ohio) and Weinland Park (Columbus,

Franklin County, Ohio) in USA to the US Environmental Protection Agency

(EPA)’s Soil Screening Levels (SSLs) and to the regional background concentrations. All of the lots in Weinland Park exceeded the natural background concentration of Pb in Franklin County (14 to 25 mg/kg soil) and 96% of the lots in Hough had Pb concentrations exceeding the background in Cuyahoga County

(56 to 136 mg/kg soil). However, when compared to the USEPA’s SSL for Pb for human ingestion of soil, only 1 out of 15 (6.6%) vacant lot in Weinland Park and

15 out of 28 (54%) in Hough neighborhood had at least one soil sample that exceeded the guidance value for Pb (400mg/kg soil). All studied sites in both neighborhoods exceeded the SSL for As (0.4 mg/kg soil); however this SSL value

15 was significantly lower than the natural background As concentrations in Ohio.

Only 1 lot out of 15 (6.6%) in Weinland Park and 3 out of 28 (11%) in Hough exceeded the background concentrations of As in Franklin (9 to 33 mg/kg soil) and Cuyahoga (5 to 20 mg/kg soil) counties. A total of 13 lots in Weinland Park had at least one soil sample with Zn concentration higher than the background range in Franklin County (71 to 177 mg/kg soil) and 23 lots in Hough exceeded the background Zn concentration in Cuyahoga County (56 to 137 mg/kg soil), however they were all within the USEPA’s SSL for Zn (23,000 mg/kg soil).

None of the vacant lots in the two neighborhoods had Cd or Cr concentrations higher than the USEPA SSLs indicating no potential human risk from the two metals. Significant correlations were observed within metals, soil properties, and between metals and soil properties including soil texture, moisture, pH, organic matter and active carbon suggesting unique associations in the two neighborhoods. Results indicate that concentrations of various metals can differ vastly between cities and Pb is a metal of concern in about 53% of the vacant lots in the Hough neighborhood in Cleveland. The study highlights the need for comparing vacant lot heavy metal concentrations to the both the USEPA SSLs and natural background concentrations in the area for establishing safety of a lot prior to its use for urban food production.

Introduction

Post-industrial cities have accumulated large masses of vacant land in the last few decades. The shutdown of primary industrial and manufacturing units in the early to mid 1900s had resulted in the downslide of the economy and rise in unemployment and poverty in several U.S. cities (Adams et al. 1993). As the working class moved to other cities in search of jobs (Adams et al. 1993), cities like Cleveland, Detroit, Youngstown and Baltimore have seen a drastic decrease in their populations (Schilling and Logan 2008). Neighborhoods witnessed an increasing percentage of vacant and abandoned structures (Schilling and Logan

2008). A lot of externalities often associated with these vacant properties such as the cost of boarding up a house, demolition of the abandoned structure, lower resale value, decrease in tax revenues and increased crime rates (Spelman 1993;

Accordino and Johnson 2000), further decreased the appeal for these cities to new families. What has been left behind in these post-industrial cities are low income populations living in sub-standard housing with often no easy access to nutritious food (Adams et al. 1993).

Due to a greater demand for local produce and need to enhance availability of fresh and healthy food particularly in economically distressed neighborhoods, coupled with the availability of vacant land in close proximity, interest in urban agriculture has increased substantially in recent years (Grewal and Grewal 2012). With diverse approaches to urban gardening including private,

17 community, municipal and educational gardens (Brown and Jameton 2000), along with several additional derived benefits such as improved human physical and psychological well-being, reduction in crime, increased employment opportunities and an increased sense of belonging (Patel 1991; Wakefield et al. 2007; Blaine et al. 2010), the fraction of land under agriculture in cities has been steadily rising.

Recent research has also indicated the high capacity of North American

“shrinking” cities such as Cleveland to increase self-reliance in fresh produce by means of urban agriculture (Grewal and Grewal 2012). However, there are concerns about human exposure to soil contamination particularly with heavy metals in these affected areas.

Earlier phases of economic expansion and urban development have resulted in significant sources of soil contamination particularly deposition of heavy metals from fossil fuel combustion from vehicles and power plants, fertilizers and pesticides, scrap paint, batteries, galvanized metal and other products (McClintock 2012; Turner and Sogo 2012; Adriano 2001; Mielke 1994).

High concentrations of heavy metals in soil in some urban areas have raised concerns over the use of this land for food production (Guo et al. 2006;

McClintock 2012) and these remnants of industrial history in cities are now becoming a threat to the existence of community gardens and neighborhood vitalization projects (Lewis 1985). There are a large number of studies in literature on the analysis of heavy metal concentrations in contaminated industrial sites or brownfields across the country (Gallagher et al. 2008; Jennings et al.

2002). Studies have shown that as distance from the city center or major roads increases, accumulation of heavy metals in the surface soil decreases (McClintock

2012; Turer and Maynard 2003; Pouyat and McDonnell 1991). However, soil contaminant information in vacant lots within urban/suburban residential areas is limited. Even more limited is the soil metal data in low income residential communities.

This study aimed to provide information on heavy metal concentrations and their relationship with soil properties in vacant lots in low income urban neighborhoods in post-industrial cities that are being targeted for urban agriculture. The specific objectives of this study were to determine: (i) the concentrations of major heavy metals in soil from vacant lots slated for urban agriculture in selected low income neighborhoods in two post-industrial cities,

Cleveland and Columbus, Ohio, USA; (ii) if these metal concentrations pose a human health risk through comparison with US EPA established Soil Screening levels (SSLs) for human ingestion of soil and the USGS provided background concentrations for the metals in the area; and (iii) the relationships between the observed metal concentrations and soil physical and chemical properties.

Materials and Methods

Description of neighborhoods and their demographics

One low income neighborhood in Cleveland and one in Columbus that had been targeted for urban agricultural expansion by the respective cities were selected for sampling in this study. The Hough neighborhood in Cleveland, Ohio, a 2 sq. mile residential area, with a dominant (more than 90%) African American population had seen a sharp decline in population and the standard of living since

1950s. The median annual income for the Hough neighborhood in 2009 was

$13,967, compared to $24,687 for the City of Cleveland and $45,395 for the State of Ohio (Cleveland City Facts 2012). About 40.8% of the population in this neighborhood has been recorded at below poverty level. Less than 40% of the children in the Hough neighborhood completed high school education while less than 10% went on for a higher degree. According to the 2010 US Census Bureau,

Cleveland had a recorded decline of 18% in its population from 2000 to 2012

(Cleveland City Facts 2012).

Weinland Park neighborhood in Columbus, Ohio, a 0.5 sq. mile residential area, has a similar demographic status with more than 50% of the population comprising of African Americans. Median annual income in the neighborhood in

2009 was $17,000, compared to $41,370 for the City of Columbus (Columbus

City Facts 2012). Around 40% of the population had not graduated from high school and 36% was out of work. Only 18% had full time jobs (Weinland Park

Community Civic Organization, 2011). The 2010 Census showed an increase in the population of Columbus by 9.6% from 2000.

Selection of vacant lots and their characteristics

Twenty eight vacant lots in the Hough neighborhood, all within a quadrant demarcated by GPS points 41.525929,-81.639318 (top left), 41.526379,-

81.608334 (top right), 41.507935,-81.621037 (bottom right) and 41.50742,-

81.639318 (bottom left) (Figure 1.1); and 15 in the Weinland Park neighborhood located within a quadrant demarcated by 39.994547,-83.004198 (top left),

39.994679,-82.996001 (top right), 39.986624,-82.996817 (bottom right) and

39.987018,-83.004198 (bottom left) (Figure 1.1) were selected for sampling. Lots located closer to schools were selected with a long term goal to engage students in urban agriculture in the future. Four vacant lots were selected close to each of the seven local schools in the Hough neighborhood in Cleveland. All the vacant lots in Columbus were around the Weinland Park Elementary School, the only school in the neighborhood. All vacant lots sampled in the Hough neighborhood were owned by the City of Cleveland whereas those in the Weinland Park were owned either privately, by the City of Columbus, or by a private company, The

Wagenbrenner Corporation. Maps of both neighborhoods showing the exact locations of the individual lots are given in Figure 1.1. Overall visual appearance and dominant plant species were recorded for each lot and are summarized below.

Vacant Lots located within Hough Neighborhood Vacant lots located within Weinland Park

Figure 2.1 Urban vacant lots in the Hough neighborhood in Cleveland, and the Weinland Park neighborhood in Columbus, Ohio

In Hough neighborhood, the vacant lots were regularly mowed every 6 –

10 days and were predominantly covered in turfgrass and associated weed species including Poa annua L. (annual bluegrass), Digitaria ischaemum S. (smooth crabgrass), Festuca arundinacea S. (tall fescue), and Taraxacum officinale L

(dandelion). Overall vegetation cover was over 90% in all the lots. In the

Weinland Park neighborhood most lots were mowed weekly with the vegetation maintained at 10 – 12 cm height, while a few were mowed less frequently. The vegetation cover included Taraxacum officinale L. (dandelion), Trifolium pretense

L. (red clover), Festuca arundinacea S. (tall fescue), Rhus typhina L. (staghorn sumac), Lythrum salicaria L. (purple loosestrife), Lonicera spp (bush honeysuckle), Sambucus Canadensis L. (american elder), Rumex obtusifolia L.

(broadleaf dock), Cichorium intybus (chicory), Phalaris arundinacea L.

(canarygrass), Elytrigia repens L. (quachgrass) and Acer negundo L. (boxelder).

Overall vegetation cover in Columbus varied between 80 - 90%.

Collection of soil samples

Soil samples were collected using a soil corer (3.5 cm diameter) from a depth of around 10 – 12 cm. In the Hough neighborhood, each vacant lot was divided into 3 approximately equal sections, with the middle section including the house foot print, and 9 soil cores were recovered from each section at random locations and combined to form a composite sample. Due to the much smaller front yards in Weinland park neighborhood, the plots were divided into 2 sections,

23 where the front section included the footprint of the house. Again, 9 cores were collected from each section at random locations and pooled into a composite sample. The samples were collected in polythene bags and kept in a cooler during transit to the laboratory, where they were stored at 4o C to prevent any changes in the nutrient and biological characteristics, until processed further. For comparison, similar composite soil samples were taken from twenty four 5ft X 7ft top soil and sub soil plots with 100% turfgrass cover from a rural land area close to freeway outside the City of Wooster, Ohio.

Identification and quantification of heavy metals in the soil

Soil samples were analyzed for heavy metal concentrations at the Soil and

Environmental Chemistry Lab, The Ohio State University, Columbus, Ohio using

Inductive Coupled Plasma - Atomic Emission Spectroscopy (ICP-AES) after acid digestion following EPA method 3051A. The soil was air dried, passed through a

2mm sieve and digested with concentrated HCl and HNO3 mixture and the resulting supernatant was analyzed using ICP-AES. Concentrations of As, Cr, Cd,

Pb and Zn were determined in mg/kg soil. The quantization limits for the metals in ICP analysis were as follows: Pb – 4mg/kg, As – 4mg/kg, Cd – 0.4 mg/kg, Cr –

4mg/kg, Zn – 4mg/kg.

Risk assessment

Soil concentration ranges of the measured heavy metals in both neighborhoods were compared with USEPA defined generic SSLs for human exposure via soil ingestion (U.S. EPA Soil Screening Guidance Technical

Background Document, Appendix A, 1996) to determine the potential risk to humans. If the metal concentration in soil was above the SSL, then it was compared with the natural background concentration ranges of these metals in their respective counties (Franklin County for Weinland Park neighborhood and

Cuyahoga County for Hough neighborhood). Data for the respective counties was obtained from the United States Geological Survey (USGS 2012). They were also compared with the natural background concentrations in Ohio and US soil published in the literature. Background concentrations for the State of Ohio were obtained from a number of individual environmental assessment reports from 64 sites across 36 counties in Ohio along with the data from the Ohio EPA (2009),

Cox and Colvin (1996), Holmgren et al. (1993), and Logan and Miller (1983).

Soil As concentrations for Ohio were also obtained from Venteris et al. (2014).

Natural background concentrations for US soil were obtained from Smith et al.

(2005), Frink (1996), Holmgren et al. (1993), Shacklette and Boerngen (1884), and Brooks (1972). Smith et al. (2005) used a series of soil samples collected in an unbiased manner from agricultural as well as non-agricultural soils at a density of 1 sample per 2000 sq. km, along transects spanning all topographic, climatic, geologic, and ecological boundaries, whereas the values presented in Holmgren et

25 al. (1993) were obtained from agricultural soils. The observed heavy metal concentrations were also compared to rural soil heavy metal values observed in

Wooster, Ohio, and the average metal concentrations in Wayne County (USGS

2012).

Estimation of traffic volumes

The number of cars passing through a busy road in the two neighborhoods was noted at the peak rush hour time between 5 and 6 pm on two different days during the week and averaged to get the mean traffic volume reading per hour for each neighborhood. A similar measurement was also taken on the freeway passing outside of Wooster, Ohio, to obtain the average traffic volume reading for a rural area.

Determination of soil physical and chemical characteristics

Soil was passed through a 2 mm sieve to remove stones and larger particles, spread on a polyethylene sheet for air-drying for 14 days at room temperature and analyzed for selected chemical and physical properties.

Antecedent soil moisture content (θv) was determined by following the gravimetric method. Particle size analysis was performed to measure the relative proportions of sand, silt, and clay for determining soil texture (Gee et al. 1986).

Soil pH was determined using a combination glass electrode in a 1:1 soil:deionized water.

Statistical Analysis

Descriptive statistical analyses for all measured parameters were performed using MINITAB v.15 (Minitab, Inc, State College, PA). All data were checked for assumptions of normality, transformed if needed, and subjected to one way ANOVA. Tukey’s comparison was used to establish significant differences in soil heavy metals and physical characteristics in the two cities at a

P value of 0.05. Principal component analysis was performed to determine clustering and grouping of variables. Pearson’s correlation helped determine significant associations within metals and within soil parameters. Multiple and linear regression analyses were used to determine important soil variables associated with the heavy metal. Since the two neighborhoods had differences in soil characteristics and relative concentrations of different metals, all data are presented separately.

Results

Soil physical and chemical characteristics

Soil characteristics varied widely in the studied sites in the two neighborhoods, amongst different vacant lots and even within individual lots (data not shown). All measured soil parameters differed significantly between the two cities at P < 0.05 (Figure 2.2). A summary of the dataset is provided in Table 1.

a a

b b

a a b

a a

Figure 2.2 Mean (+ SE) for soil characteristics measured in vacant lots in Weinland Park (Columbus) and Hough neighborhoods (Cleveland), Ohio. Means (bars) with different letters are significantly different (Tukey’s mean comparison) at P < 0.05.

Continued

Figure 2.2 continued

Mean Minimum 25th PCTL Median 75th PCTL Maximum Variable Hough WP Hough WP Hough WP Hough WP Hough WP Hough WP As (mg/kg soil) 12.02 21.51 5.16 13.89 9.26 17.88 10.82 20.71 13.21 24.82 35.1 38.46 Cd (mg/kg soil) 1.13 1.65 0.36 0.75 0.78 1.15 0.99 1.48 1.19 2.07 3.62 4.36 Cr (mg/kg soil) 18.41 23.31 9.09 16.87 13.68 19.01 16.32 22.04 22.83 24.88 46.25 58.6 Pb (mg/kg soil) 334.1 123 56.9 21.7 188.2 80.5 280.5 115.1 407.8 180.9 1178 1004 Zn (mg/kg soil) 203.6 253.2 84.1 126.8 146.6 168 182.2 234.9 241.3 310.2 634 545.4 30 % Clay 9.47 26.21 4.12 9.99 6.11 18.95 7.83 24.67 10.98 33.68 33.16 47.58 % Sand 69.4 12.04 40.18 7.47 61.39 10.54 73.7 12.22 76.44 13.22 92.35 17 % Silt 21.14 61.75 0.0 39.76 16.16 54 18.94 63.44 26.26 68.12 50.41 81.02 pH 6.97 7.52 6.24 7.25 6.75 7.45 7.07 7.52 7.16 7.57 7.46 7.77 % Moisture 8.24 31.71 1.5 23.88 4.42 27.65 6.72 30.03 10.25 33.64 20.47 55.88 % SOM 4.23 6.7 2.0 0.0 3.25 5.45 3.96 6.53 4.89 7.86 7.26 14.76 C (mg/kg soil) 636.05 1190 413.28 0.0 604.22 898 657.47 898 690.82 1400 694.8 4916

The lots studied in Weinland Park had higher clay and silt content ranging from

10 to 47.5% and 46.8 to 81%, respectively, while those in Hough had higher sand content ranging from 40.1 to 92.3%. Soil pH in Weinland Park varied from 7.25 to 7.77, while in Hough it varied from 6.24 to 7.46. Hough soil samples were comparatively dry with antecedent soil moisture varying from 1.5 to 20.5%, whereas the moisture ranged between 24 and 56% in the Weinland Park samples.

Soil organic matter varied from 0 to 14% and active carbon content from 0 to

4916 mg/kg soil in Weinland Park neighborhood which were significantly higher than the Hough neighborhood. The highest variation within a single vacant lot was observed in soil texture with clay and silt varying by almost 34% between the different sections.

Soil heavy metal concentrations

Concentrations of all the heavy metals in soil differed significantly between the two cities at P < 0.05 (Figure 2.3). Soil As concentrations were significantly higher in Weinland Park, when compared with Hough neighborhood and Wooster soil concentrations (Table 2.2). The range of soil As concentration in

Hough neighborhood (5.2 to 31.1 mg/kg soil) was higher than the maximum concentration observed in the Cuyahoga County (5.4 to 19.9 mg/kg soil), however the 75th percentile value of 13.21 mg/kg soil was within this range. Range of soil

As in Weinland Park neighborhood (13.9 to 38.5 mg/kg soil) was close to the

a a

b b

a a b

Figure 2.3 Mean (+ SE) concentrations of heavy metals measured in vacant lots in Weinland Park (Columbus) and Hough neighborhoods (Cleveland), Ohio. Means (bars) with different letters differ significantly (Tukey’s mean comparison) at P < 0.05.

Values As Cd Cr Pb Zn Franklin County (USGS, 2012) 17.79 NA NA 18.28 104.64 Cuyahoga County (USGS, 2012) 12.59 NA NA 21.14 101.88 Wayne County (USGS, 2012) 12.87 NA NA 19.09 67.08 Ohio (Venteris et al., 2014) 9.26 NA NA NA NA Ohio (OEPA 2009) NA 1.25 22 37 90 Ohio (Cox and Colvin 1996) 5.72 0.51 12.1 16.2 42.7 Ohio (Holmgren et al, 1993) NA 0.36 NA 18.2 82.1 Ohio (Logan and Miller 1983) NA 0.2 12 19 75 US (Smith et al., 2005) 5.74 0.3 71.3 22.08 58.02 US Northeast (Frink 1996) NA 1 36 14 36 US (Holmgren et al 1993) NA 0.27 NA 12.3 56.5 US East (Shacklette & Boerngen 1984) 4.8 NA 3.3 14 40 US (Brooks 1972) 5 NA 200 10 50 Hough neighborhood, Cleveland, Ohio (this study) 12.02 1.13 18.41 334.1 203.6 Weinland Park neighborhood, Columbus, Ohio (this study) 21.51 1.65 23.31 158.3 253.2 Freeway, Wooster, Ohio (this study) 10.52 0.93 23.65 24.35 98.51

33 range observed in Franklin County (9.1 to 33.5 mg/kg soil) with the 75th percentile value within this range (USGS 2012). Range of Pb concentration in

Hough neighborhood (56.9 to 1178 mg/kg soil) was significantly higher than the natural background range in Cuyahoga County (12.3 to 31.9 mg/kg soil) and soil

Pb concentration in Weinland park neighborhood (21.7 to 1004 mg/kg soil) was significantly higher than background range in Franklin County (14 to 25.3 mg/kg soil) (USGS 2012). Mean Pb concentration in Hough was significantly higher than that in Weinland Park and the two neighborhoods had Pb concentrations exceeding rural, Ohio and US mean values by almost a factor of 10. More than

80% of the soil samples in both Hough and Weinland Park neighborhoods exceeded the background Zn concentrations in Cuyahoga county (56 to 136.9 mg/kg soil) and Franklin county (71.6 to 177 mg/kg soil), respectively. Weinland

Park also had a mean Zn concentration significantly higher than Hough and both neighborhoods had soil Zn concentrations significantly higher than the rural

(Wooster) Ohio and U.S. background Zn values. Weinland Park mean Cd concentration was significantly higher than mean Ohio and U.S. background values, whereas the means in Hough and Wooster were comparable and fell within the background concentrations. Mean soil Cr concentrations in Weinland

Park and Hough neighborhoods were comparable and lower than the mean rural,

Ohio and U.S. background concentrations.

Risk assessment

Soil heavy metal concentrations in the two neighborhoods along with the generic SSLs established by the USEPA for exposure to humans via soil ingestion

(USEPA 1996) and the regulatory guidance values for each metal in residential soil set by the OEPA (2009) and USEPA (2003) are presented in Table 2.3.

Cadmium, Cr and Zn concentrations in both the neighborhoods were within all regulatory limits and soil ingestion SSLs. All the sites had at least one soil sample with As concentration higher than the USEPA SSL and USEPA guidance value of 0.4 mg/kg soil and OEPA VAP of 6.7 mg/kg soil. Only 6% of the vacant lots (1 out of 15) in Weinland Park and 53% in Hough neighborhood (15 out of

28) had at least one sample with soil Pb concentrations higher than the USEPA

SSL, and OEPA and USEPA guidance value of 400 mg Pb/kg soil (Table 2.3).

Relationship between soil characters and metal concentrations

Hough Neighborhood

Principal component analysis revealed strong correlations the soil properties and metals (Figure 2.4). Strong clustering was observed between the heavy metal concentrations and organic matter and active carbon content. Soil moisture and pH were also grouped together. Cd, Cr, Pb Zn, % sand, and %silt were the important contributors to the 1st principal component with maximum negative loading from % sand and maximum positive loading from Zn

As Cd Cr(III) Cr(VI) Pb Zn USA (USEPA 2003) 0.4 37 100,000 30 400 23,000 Ohio (OEPA 2009) 6.7 70 120,000 230 400 23,000 Generic SSLs 0.4 78 NA 390 400 23,000

0.5 Clay % M 0.4 pH

t 0.3

n Silt % e

n 0.2

o p

0.1

o C

0.0 As d

n Pb

-0.1 C

o c

e -0.2 Zn

S OM Cd Cr -0.3 Sand%

-0.4 -0.4 -0.3 -0.2 -0.1 0.0 0.1 0.2 0.3 0.4 First Component

Figure 2.4 Principal component analysis (PCA) loading plot for the 1st and 2nd component axis for heavy metal concentrations and soil physical and chemical parameters in the Hough neighborhood in Cleveland, Ohio. M = % soil moisture and OM = % organic matter

concentration. Percent clay and % soil moisture gave the maximum loading on the 2nd principal component axis. The first two components together explained

50% of the variability in the dataset. Correlation analysis revealed significant positive correlations between all the heavy metals (P < 0.05) except that of As with Pb and Zn concentrations, which were weakly correlated. All the measured soil properties were highly correlated with positive correlations between soil silt and clay fractions and negative correlation with sand (P < 0.05). Soil moisture was positively correlated with % clay (P = 0.02). Organic matter was positively correlated with % clay (P = 0.03) and % silt (P = 0.004) as well as active carbon

(P < 0.001), whereas negatively correlated with % sand (P = 0.007).

Multiple regression analysis revealed that none of the measured soil properties contributed to the variation in As concentrations, however linear regression showed that % clay (F = 4.63; df = 1, 48; P = 0.036) and organic matter content (F = 4.86; df = 1, 52; P = 0.032) were significantly correlated with

As concentrations in the Hough neighborhood. Similarly for Cd concentrations, all soil parameters together did not produce any significant relationship; however, individual analysis with the soil properties showed that % silt was significantly correlated with Cd (F = 7.66; df = 1, 48; P = 0.008). Organic matter was correlated with Cr concentration (F = 5.19; df = 1, 45; P = 0.028) when analyzed with all other soil properties, but, individual analysis also showed that soil pH (F

= 4.30; df = 1, 54; P = 0.042), % silt (F = 6.79; df = 1, 51; P = 0.01), % sand (F =

8.69; df = 1, 50; P < 0.005), and soil active carbon (F = 10.04; df = 1, 52; P =

0.003) were correlated with Cr concentrations. None of the soil parameters were correlated to Pb concentration when analyzed together, however, individual analysis showed % sand (F = 4.26; df = 1, 47; P = 0.045) was significantly correlated with soil Pb. Finally for Zn, none of the soil parameters showed a significant relationship, whereas soil pH (F = 6.61; df = 1, 53; P = 0.013), organic matter (F = 8.35; df = 1, 53; P = 0.006) and soil active carbon (F = 9.57; df = 1,

51; P = 0.003) were correlated to Zn in the individual analysis. Degrees of freedom vary for the different soil parameters due to removal of outliers to achieve normality.

There were no differences in any of the measured metal concentrations or soil properties between the different sections of the vacant lots.

Weinland Park neighborhood

Principal component analysis showed strong clustering between the metal concentrations in the Weinland Park neighborhood however, As was not a strong contributor to this group (Figure 2.5). Organic matter, soil pH and moisture were also present as a separate group. Important variables with maximum loading to the 1st principal component were Cd, Zn Cr, and Pb. Percent clay and silt were important contributors with maximum loading on the 2nd component. The first two components explained 48% of the variability in the dataset.

As observed with the Hough neighborhood, there were significant positive correlations between different heavy metals (P < 0.05) in Weinland Park, except

0.75 %silt

0.50 OM

t pH

n e

n 0.25

o Moisture p

m C Zn

o Pb

C Cr Cd

0.00 As d

n %sand

o c

e -0.25 S

-0.50 %clay

-0.3 -0.2 -0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 First Component

Figure 2.5 Principal component analysis (PCA) loading plot for the 1st and 2nd component axis for heavy metal concentrations and soil physical and chemical parameters in Weinland Park neighborhood in Columbus, Ohio. OM = % organic matter.

As which was not significantly correlated with any of the other heavy metals.

Among soil parameters, % silt was negatively correlated with % clay (P < 0.001).

Soil organic matter was negatively correlated with % clay (P = 0.02) and positively with % silt (P = 0.04) and soil moisture (P = 0.03). Soil carbon content was significantly correlated with As concentration in Weinland Park in a multiple regression analysis (F = 4.98; df = 1, 23; P = 0.03). When analyzed individually, none of the other variables had a significant relationship with soil As concentration. No soil parameter was correlated with Cd, Cr, Pb or Zn concentrations in soil when analyzed together or individually except organic matter, which showed a positive correlation with Zn (F = 4.55; df = 1, 27; P =

0.043).

One way analysis of variance showed significant difference between soil pH in the front and backyard portion of the vacant lots (F = 3.86; df = 2, 21; P =

0.04). However, there was no difference in any of the other measured parameters.

Traffic Volumes

The traffic volume data showed that there were 1,369 vehicles/hour for the

Hough neighborhood, 1,672 for Weinland Park neighborhood, and 813 for

Wooster, Ohio. Vehicles passing adjacent to the targeted sampling site in

Wooster were mainly bigger semi-trucks whereas those passing through the two residential neighborhoods were mainly cars.

Discussion

We used the USEPA SSLs for direct ingestion of soil by humans as our first level of screening to determine whether metal concentrations in vacant lots in

Weinland Park and Hough neighborhood were of any potential risk to humans.

Our comparison of soil As concentrations in vacant lots to the USEPA SSL of 0.4 mg/kg soil indicated a possible contamination in all the studied sites. However, this SSL for soil As is a conservative value that is back-calculated for carcinogenic risk to humans based on the assumption that approximately 100% of the soil As is bioavailable. This leads to an overly conservative estimate lower than even the natural background concentrations of As in Ohio or U.S. soils

(Venteris et al. 2014). Also, the soil ingestion pathway values are developed keeping in mind the most susceptible population of children younger than 6 years of age adding additional bias to the equation in the form of body weight and daily soil ingestion rates (USEPA 1996). Additionally, the national guidance values are determined using EPA method 3050B which is more aggressive in extracting metal fractions from soil that may not be extracted in the human gastro-intestinal tract (Jennings 2008). Moreover, the natural background concentrations of As in

Franklin (9 to 33mg/kg soil) and Cuyahoga (5 to 20 mg/kg soil) counties are significantly higher than the SSL of 0.4 mg/kg soil. Background metal concentrations depend on the bedrock geochemistry and mineral composition in a given area (Adriano 2001; Kabata-Pendias 2000; Rieuwerts et al. 1998). High As

42 background concentrations in the two counties may originate from the shale parent bedrock material found in these geographic areas (Venteris et al., 2014).

This study showed that only 6.6% of the vacant lot in the Weinland Park neighborhood and 11% in the Hough neighborhood had at least one soil sample with As concentrations higher than the maximum natural background concentration in the respective counties, thus posing a potential human exposure risk. This may be due to a combination of the bedrock geochemistry and industrial past of the neighborhoods consisting of iron, coal and textile industries in

Franklin County and automobile industries in Cuyahoga County (Warf and Holly

1997; Jennings 2008). Although most heavy metal studies in urban areas do not include soil As analysis, its use in the form of chromate copper arsenate (CCA) treated wood for construction may be a source of contamination in urban soil

(Girouard and Zagury 2009; Belluck et al. 2003). Based on our results and the above discussion, we conclude that 93% of the lots in Weinland Park (Columbus,

Ohio) and 89% in Hough neighborhood (Cleveland, Ohio) are free from As contamination.

A comparison with USEPA SSL for Pb showed that only 1 vacant lot out of 15 (6.6%) in Weinland Park and 15 out of 28 (54%) in Hough neighborhood had at least one soil sample with Pb concentration exceeding the SSL of 400 mg/kg soil, thus posing a potential human exposure risk via ingestion of soil.

When compared to the natural background concentrations, at least one soil sample from all vacant lots in both Weinland Park and Hough neighborhoods exceeded

43 the maximum concentration observed in Franklin (14 to 25 mg/kg soil) and

Cuyahoga (56 to 136 mg/kg soil) counties. There were no significant differences in the level of Pb contamination between the different sections of the vacant lots in either neighborhood. A potential anthropogenic source of excessive soil Pb in and around densely populated cities is high vehicular traffic (USEPA 1998;

Pouyat and McDonnel 1991; Charlesworth et al. 2003). The traffic densities in the two residential neighborhoods at 1,369 to 1,672 vehicles/hour were almost double the volume of traffic on a highway observed in a rural area around Wooster, Ohio.

The traffic densities may have been even higher when the two neighborhoods were a part of thriving industrial townships in the past, with greater contributions to Pb particles in air through exhaust and industrial emissions that settled down on the surrounding land area. Another anthropogenic source of Pb containing dust is improper practices such as removal of Pb paint from houses by power sanding and scraping that generates lead dust (USEPA 1998; Mielke et al. 2001). A large number of houses in these neighborhoods are vacant and ready for demolition while many others have been taken down in the recent past. The City of

Cleveland has spent $47 million in the last decade on demolition and is awaiting more federal funds to tear down close to 8,500 distressed houses (Sweeney and

Brancatelli 2012). Paint dust falling directly on the soil from house demolition is a primary source of not only Pb but also of other metals found in paint such as Zn,

Cd, Ni and Cr (Mielke et al. 2001).

Even though approximately 86% of the vacant lots in Weinland Park and

89% in Hough neighborhood had Zn concentrations higher than the natural background concentrations in Franklin (71 to 177 mg/kg soil) and Cuyahoga (56 to 137 mg/kg soil) counties respectively; none of the lots had Zn concentration higher than the USEPA SSL for human ingestion of 23,000 mg/kg soil. Thus Zn is not a metal of concern in these vacant lots since it can be regulated in the human body through metabolism and hence, low concentrations do not pose any risk to children or adults (Nriagu 2007; Duruibe et al. 2007). Concentrations higher than background levels may be due to the paint dust or the use of galvanized housing construction material (Turner and Sogo 2012; Mielke et al.

2001). None of the vacant lots in the two neighborhoods had Cd or Cr concentrations higher than the USEPA SSLs indicating no potential human risk from the two metals.

The USEPA and various state EPAs have established regulatory guidance values for multiple soil metal contaminants based on soil surveys, to be taken into consideration when devising remediation plans for a contaminated site. Jennings

(2008) compiled the guidance values proposed by 30 different US states and concluded that there exist vast variations even within neighboring states due to differences in assumptions, sampling procedures, methodologies, metal extractions procedures and the parent bedrock geochemistry; and hence comparison to these values should not be the only criteria for the need of the remediation plan. To cover the entire range of background metal concentrations in

Ohio and US soil, we examined multiple published sources (as presented in Table

2), however comparisons with the Franklin and Cuyahoga county background metal concentrations were found to be most relevant. A more appropriate estimation of risk can be made if the bioavailable or plant tissue concentrations of the metals are available. Based on our analysis, we conclude that only Pb concentrations particularly in the Hough neighborhood in Cleveland exceed the

SSLs for human ingestion of soil in 54% of the vacant lots. However, plant tissue bioassays and Pb bioavailability analysis can shed further light on the actual human exposure risk via ingestion of plant material or soil in the contaminated lots.

Overall, vacant lot soil heavy metal concentrations in the two low income residential neighborhoods may be attributed to 4 main causes: (i) parental bedrock geochemistry in the two geographic regions of the state of Ohio; (ii) industrial past and contamination with wastes and stack fumes; (iii) vehicular exhaust and; and (iv) metals in the exterior paint on houses. Significant positive correlations within metals could be explained by their co-occurrence in soil, possibly arising from the same source and hence a study of their cumulative effects is essential for formulating remediation strategies. Metal availability in soil is also governed by its mineralogical profile which is difficult to determine in urban areas that have undergone extensive disturbance (Ge et al. 2000), and therefore it is necessary to explore the relationships of metals with the soil parameters before concluding the soil as contaminated.

This study showed large variability in soil physical characteristics in vacant lots in both neighborhoods. Soil properties showed strong correlations among themselves in the Pearson’s correlation analysis and grouping in the principal component analysis. In the Hough neighborhood with more sandy, dry soils with a lower organic matter and active carbon content, we found that soil texture, pH and organic matter were strongly correlated with the heavy metal concentrations. Soil texture (especially % clay) and soil pH play an important role in determining the mobility and bioavailability of heavy metals (Adriano 2001;

Kabata-Pendias 2000; McGowen et al. 2001). The neutral to alkaline soil in

Weinland Park neighborhood would hold the metal in a complex form with the solid phase rendering it immobile and slightly more stable (Moller et al. 2005;

Rieuwerts et al. 1998), whereas it would remain free from the soil particles and other minerals in acidic soil. Organic matter was significantly correlated with the metals in Weinland Park neighborhood. Organic matter can make the metals more stable in soil by limiting their mobility by chelating them with humic acids

(Erdogan et al. 2007). Higher organic matter content in Weinland Park neighborhood with greater proportion of clay in soil may contribute to greater metal stability as opposed to the Hough neighborhood with more sand and less organic matter. In conclusion, multiple soil properties may govern the behavior and bioavailability of metals in soil and their inter-relationships demand a thorough analysis taking into consideration all metals, soil parameters and their inter-correlations.

Increase in vacant property is synonymous with decrease in market demand and decline in businesses in the area. Hence, making use of the empty land parcels may decrease a city’s cost of maintaining the vacant property and help improve the overall aesthetic appeal and economic condition of the neighborhoods which is important for attracting new residents, businesses and redevelopment initiatives (Accordino and Johnson 2000). The spurred economic growth can subsequently lead to improvements in the standard of living

(Grossman and Krueger 1995). Although heavy metal contamination in

Cleveland is a well acknowledged concern for brownfields and industrial sites

(Petersen et al. 2006; Jennings et al. 2002), this study extends this concern to residential vacant lots in Cleveland and Columbus, and calls for a more cautious approach for using this land.

The most direct impact of soil metal contamination in low income neighborhoods is the use of these vacant lots for urban agriculture. A variety of social, economic and educational factors can affect the diet of a household or community (Diez-Roux et al. 1999; Winkler et al. 2006). People living in a low income neighborhood are less likely to include nutritious fruits and vegetables in their everyday meals (Diez-Roux et al. 1999) due to the lack of affordability, absence of private vehicles to reach the supermarket or the cost of travel to a faraway store exceeding the cost of less nutritious food available close-by

(Winkler et al. 2006). Hence, the residents in such neighborhoods would benefit tremendously from a local source of fresh vegetables and fruits to supplement

48 their diet and gain all associated health benefits. The results of this study show that each urban lot targeted for urban agriculture should be evaluated for potential metal contamination due to micro-scale variation in metal concentrations and soil physical and chemical properties to avoid potential health risks associated with dust inhalation and intake of contaminated produce. Although metal contamination risk is possible in other cities around the world, differences in local bedrock mineralogical composition and other soil properties can affect metal bioavailability differently.

In conclusion, results from this study showed that all of the vacant lots in the two disadvantaged neighborhoods were not contaminated with heavy metals.

We found only Pb and Zn concentrations to be higher than their natural background concentration ranges. However, Pb concentration in only one vacant lot out of the 15 studied in Weinland Park and in only 15 out of the 28 lots studied in Hough neighborhood, exceeded the USEPA established SSL of 400 mg/kg soil.

Hence further targeted investigation is required with respect to Pb bioavailability in soil and plant uptake in these lots. Also, comparison of vacant lot soil As concentrations with the SSL of 0.4 mg/kg soil was not relevant due to naturally higher background concentrations for As in both the counties. Therefore, to establish potential human risk from heavy metal contamination in vacant lot, we propose comparisons with the USEPA established SSLs for human ingestion of soil and the natural background soil metal concentrations for the respective counties as determined by the USGS. If the metal concentrations are below these

49 values, it may be safely used for growing food. However, if the metal concentrations are higher than these values, then further investigation is required to assess metal bioavailability to plants and its uptake in the food chain. Soil properties such as acidic pH, low organic matter content and a lower proportion of clay may additionally contribute to greater metal availability and hence, vacant lots with these properties may also require plant tissue assays and bioassays on edible fruits and leaves.

Acknowledgements

We would like to thank the Cleveland Planning Commission and the Hough neighborhood Land Bank for help with the identification of city owned lots in

Cleveland for sampling, and the Weinland Park Neighborhood Association, Mid-

Ohio Regional Planning Commission, and The Wagenbrenner Corporation for permission to sample vacant lots in the Weinland Park Neighborhood in

Columbus. We also thank U.S Department of Housing and Urban Development along with the Food Innovation Center Grant for funding, Dr. Rafiq Islam of the

Ohio State University for analyzing the active carbon data, and Dr. Zhiqiang

Cheng, Mr. Kevin Power and Priyanka Yadav of the Urban Landscape Ecology program of the Ohio State University for assistance with sampling.

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Chapter 3: Relationship between heavy metal contamination and soil food web health in vacant lots slated for urban agriculture in two post-industrial

cities

Abstract

Urban agriculture offers a means of obtaining healthy food while making use of vacant land in cities. However, soil contamination with heavy metals is a major concern for human health, food safety and soil food web health. In a previous study we reported on the human health risks of heavy metal contamination in soil in 43 vacant lots in two low-income neighborhoods, Hough and Weinland Park, located in two post-industrial cities, Cleveland and Columbus

(Ohio, USA), respectively. In this study, we determined the relationship between heavy metal concentrations and the soil food web health using nematode community as a surrogate in the same lots. A general absence of higher trophic level omnivorous and predatory nematodes and an over-abundance of plant- parasitic nematodes indicated the disturbed nature of the urban soil food web.

When compared to the USEPA’s Ecological Soil Screening levels (Eco SSLs) only Zn was established as a metal of concern for soil invertebrates and it was found to be negative associated with Channel index in the multiple regression

57 analysis. Principal component analysis revealed different clustering of heavy metals, soil properties and nematode parameters in the two cities indicating unique associations. Multiple regression analysis revealed a combination of As,

Cd, Cr, soil texture and organic matter as significant factors associated with nematode abundance and community indices. Bacterivore and fungivore nematodes were negatively correlated with As and positively with Cd and Cr; whereas plant parasitic nematodes were positively correlated with Cr, % silt and active carbon content, perhaps due to the influence of these heavy metals on the nematode food sources. Soil Pb and Zn concentrations that were elevated in these vacant lot beyond natural background concentrations did not show any significant associations with the nematode community; whereas the metals present within background concentration, i.e., As, Cd and Cr were correlated with the opportunistic bacterivore and fungivore nematodes. Results showed that soil As concentrations were negatively associated with the lower trophic level nematodes in Hough neighborhood. Additionally, strong correlations between As, Cd, Cr, organic matter and soil texture influenced the nematode population densities.

Introduction

Lack of access to healthy food (due to constraints associated with availability and affordability) has given rise to hunger and obesity simultaneously in low income urban neighborhoods in North America (Larsen and Gililand 2008;

Schneider 2008; Zenk et al. 2005). Urban agriculture is increasingly being considered as a potential solution to address both food insecurity and malnutrition, especially in post-industrial Midwestern cities where vacant land has rapidly accumulated due to the recent home foreclosure crisis (Grewal and

Grewal 2012; Schilling and Logan 2008; Adams et al. 1993). However, there are concerns about the ability of urban soils to sustain food production due to the extensive soil disturbance associated with human activities including construction and demolition of buildings and other land use activities. In fact, residual construction materials from the building and foundation, including bricks, stones, metals and wood, along with stripped paint are often left on site or buried in the soil (Park et al. 2010; Cheng et al. 2008). Additionally, there are concerns about potential contamination of urban soils, especially with heavy metals, which may pose risks to humans (Sharma et al. 2014) and to soil organisms which provide beneficial ecosystem services such as organic matter decomposition and biological pest and disease regulation. Therefore, if this vacant land is to be used for urban agriculture, both human health risks and soil health need to be addressed

(Knight et al. 2013; Grewal et al. 2011).

In a previous study, we assessed the extent of heavy metal contamination in soil in two post-industrial cities, Cleveland and Columbus (Ohio, USA), and determined its potential human health risk (Sharma et al. 2014). In this study, we determined the relationship between soil heavy metal contamination and the soil food web health in these same cities. We used soil nematode community as a

59 surrogate for the soil food web as nematodes are important components of the soil food web, affecting energy transfer, nutrient transformation and organic matter decomposition (Chen et al. 2009; Ferris et al. 2001). They are well adapted to a wide range of environmental conditions and respond rapidly to changes or disturbances in the ecosystem (Yeates and Bongers 1999; Coleman et al. 2004).

Small size, abundance, trophic diversity, occurrence in all soil types, short life cycles, and visible internal anatomy makes nematodes particularly useful environmental bioindicators (Briar et al., 2008; Shao et al. 2008; Ferris and

Bongers 2006). Commonly found heavy metals including Arsenic (As), Lead

(Pb), Cadmium (Cd), Chromium (Cr) and Zinc (Zn) have been shown to affect nematodes in soil (Bongers and Bongers 1998; Georgieva et al. 2002, Korthals et al. 1996). Studies have reported higher trophic level omnivorous and predatory nematodes such as Dorylaimina and Mononchina as being particularly sensitive to lead pollution (Zullini et al. 1985; Pen-Mouratov et al. 2008). However, there are no reports on the influence of heavy metal contamination on the soil nematode community in disturbed urban ecosystems.

The main goal of this study was to determine the relationship between heavy metal contamination and soil food web health using the soil nematode community as a surrogate for the soil food web in low income neighborhoods in

Cleveland and Columbus which are being targeted for urban agriculture. We previously documented the concentrations of heavy metals As, Cd, Cr, Pb and Zn along with soil texture, pH, moisture and organic matter content in 43 vacant lots

60 in two low income neighborhoods, Hough (Cleveland) and Weinland Park

(Columbus) (Sharma et al. 2014, in press). The specific objectives of this study were to (i) analyze the soil nematode communities in the vacant lots in Hough and

Weinland Park residential neighborhoods; (ii) compare the soil heavy metal concentration in the lots to USEPA established Ecological Soil Screening Levels

(Eco SSLs) for the metals to determine risk to soil invertebrates and (iii) identify variables from soil properties and heavy metals that are significantly correlated with the soil nematode abundance and community parameters using multiple regression analysis.

Materials and Methods

Two disadvantaged neighborhoods, one each in Cleveland and Columbus,

Ohio, were selected for this study. Twenty eight vacant lots were sampled in the

Hough neighborhood in Cleveland and fifteen in the Weinland Park neighborhood in Columbus, which were being considered for food production by various neighborhood organizations. Detailed descriptions of the neighborhoods and vacant lots are provided in Sharma et al. (2014, in press), along with the procedures followed for collection of soil samples and determination of soil physical and chemical characteristics, and identification and quantification of heavy metals. These heavy metals and soil physical and chemical properties, referred to as environmental variables (or predictor variables) hereafter in this

61 study, were used to determine their relationships to the nematode community parameters.

Nematode extraction and identification

Nematodes were extracted from 10 g fresh soil taken from the composite samples collected from each vacant lot, using the Baermann funnel technique

(Flegg and Hooper 1970) at 22 OC over a period of 72 hours. They were heat killed at ~50oC. Nematodes were observed with the help of an inverted stereo microscope and a gridded petriplate where the first 100 were indentified to the genus level using the ‘Interactive diagnostic key to plant parasitic, free-living and predaceous nematodes’ made available by the University of Nebraska Lincoln,

Nematology Lab, based on original publication by Tarjan et al. (1977). The remaining nematodes were counted to give the total number in each sample.

Nematode community analysis

Each nematode genus was classified into one of five tropic groups: bacteria feeding (BF), fungus feeding (FF), plant parasitic (PP), predatory (PR), and omnivorous (OM). The number of genera in each sample was estimated based on the first 100 individuals identified. Each genus was also classified along the colonizer-persister (c-p) scale from 1 to 5 following Bongers (1990). Various nematode community indices including the maturity index (MI), plant-parasitic index (PPI), combined maturity index (CMI), enrichment index (EI), channel

62 index (CI) and structure index (SI) were calculated, along with Shannon’s diversity index, Menhinic’s richness index and evenness index (Yeates 1994;

Bongers 1990; Ferris et al. 2001).

Risk assessment for nematode community

Vacant lot heavy metal concentrations were compared to the USEPA established Ecological Soil Screening Levels (Eco SSLs) of the metals with respect to exposure to soil invertebrates (USEPA, 2005).

Statistical analysis

Descriptive statistical measures were determined for all parameters.

Nematode count data was transformed using log transformations to meet the assumption of normality before performing analyses. All nematode community parameters and calculated indices were compared between the two neighborhoods using ANOVA and Tukey’s comparison at a P value of 0.05. Principal

Component Analysis (PCA) was used to look for grouping of correlated variables.

Multiple linear regression analysis using the ‘best-subsets’ approach was performed on the soil heavy metals, physical and chemical properties and nematode counts and community indices from the two neighborhoods, to identify a combination of environmental variables that would best explain the variations in the nematode communities in both Weinland Park and Hough neighborhoods. All

63 statistical tests were performed using MINITAB v.16 (Minitab, Inc, State College,

PA).

Results

Table 3.1 lists the means, standard errors (SE) of means, and the ranges of all the heavy metals, soil properties, and nematode abundance and community indices recorded in the two neighborhoods. A total of 34 nematode genera were identified from all the samples in Weinland Park and Hough neighborhoods

(Table 3.2) with total abundance in Weinland Park varying from 27 to 359 nematodes per 10 g soil and in Hough neighborhood from 38 to 988 nematodes per 10 g soil. Bacteria feeding nematodes belonging to genera Rhabditus,

Panagrolaimus, Cephalobus, and Acrobeloides and plant parasitic nematodes of genera Filenchus and Pratylenchus were found in highest numbers. Comparison between the two neighborhoods revealed that the total abundance of nematodes was higher in the Hough neighborhood. Nematodes belonging to c-p scale 1, 2 and 3, and bacteria and fungus feeding nematodes were also found in greater abundance in the Hough neighborhood (Figure 3.1). Among the various community indices EI, SI, Menhinic's richness index and evenness index were higher in Weinland Park; whereas CI and PPI were higher in the Hough neighborhood (Figure 3.2).

Weinland Park Hough Neighborhood Variable Mean SE Mean Minimum Maximum Mean SE Mean Minimum Maximum Arsenic 21.5 0.9 13.9 38.5 12.0 0.7 5.2 35.1 Cadmium 1.6 0.1 0.7 4.4 1.1 0.1 0.4 3.6 Chromium 23.3 1.4 16.9 58.6 18.4 1.0 9.1 46.2 Lead 158.3 31.4 21.7 1004.0 334.1 23.7 56.9 1178.0 Zinc 253.2 18.5 126.8 545.4 203.6 12.2 84.1 634.0 % Clay 26.2 1.8 10.0 47.6 9.5 0.6 4.1 33.2 % Sand 12.0 0.4 7.5 17.0 69.4 1.3 40.2 92.4 % Silt 61.8 1.8 39.8 81.0 21.1 0.9 0.0 50.4

65 pH 7.5 0.0 7.3 7.8 7.0 0.0 6.2 7.5 % Moisture 31.7 1.2 23.9 55.9 8.2 0.6 1.5 20.5 SOM 6.7 0.5 -1.1 14.8 4.2 0.1 2.0 7.3 Active Carbon 1190.0 196.0 -106.0 4916.0 636.1 7.3 413.3 694.8 Total nematode population 158.2 15.8 27.0 359.0 243.5 18.6 38.0 988.0 Total genera diversity 15.4 0.6 6.0 21.0 15.6 0.3 7.0 20.0 Free living nematodes 107.6 12.9 25.9 331.6 187.3 15.7 22.0 851.0 Plant parasitic nematodes 50.6 7.5 1.1 180.4 56.2 5.4 6.0 375.4 Bacteriovores 82.5 9.7 14.0 225.7 139.8 11.4 16.0 606.5 Fungivores 17.8 3.6 1.0 88.9 41.0 4.4 0.0 234.8 Omnivores 6.2 1.0 0.0 17.1 5.7 0.8 0.0 35.8 Predatory 1.0 0.2 0.0 5.0 0.8 0.2 0.0 9.5

Continued

Table 3.1 continued

Maturity Index 1.6 0.0 1.2 2.0 1.6 0.0 1.3 2.1 Plant parasitic index 2.4 0.0 2.0 3.0 2.4 0.0 2.0 3.0 Combined maturity index 1.8 0.0 1.4 2.2 1.8 0.0 1.5 2.4 Enrichment index 85.4 1.3 67.9 96.1 78.9 0.9 53.5 93.6 Structure index 39.9 4.1 0.0 77.4 20.0 2.1 0.0 77.4 Channel index 7.0 0.9 1.0 18.7 10.6 0.6 0.0 29.4 Menhinic Richness index 1.4 0.1 0.6 2.4 1.2 0.0 0.5 2.3 Shannon's Diversity index 2.2 0.0 1.4 2.6 2.3 0.0 1.8 2.7 Evenness Index 0.8 0.0 0.7 0.9 0.2 0.0 0.1 0.3

Table 3.2 List of nematode genera identified and their assigned colonizer- persister scale values (numbers in parenthesis, following Bongers 1990) from soil samples collected from vacant lots in the Hough (Cleveland, Ohio) and Weinland Park (Columbus, Ohio) neighborhoods

Bacterivores Fungivores Predators Omnivores Plant Parasites

Acrobeles (2) Aphelenchoides (2) Mononchus (4) Dorylaimus (4) Aglenchus (2) Acrobeloides (2) Aphelenchus (2) Eudorylaimus (4) Criconemoides (3) Cephalobus (2) Nygellus (4) Filenchus (2) Chiloplacus (2) Pungentus (4) Helicotylenchus (3) Diplogaster (1) Heterodera (3) Eucephalobus (2) Hoplolaimus (3) Monhystera (1) Longidorous (5) Panagrolaimus (2) Mesocriconemoides (3) Pelodera (1) Paratylenchus (2) Plectus (2) Pratylenchus (3) Rhabditis (1) Psilenchus (2) Wilsonema (2) Rotylenchus (3) Alaimus (4) Tylenchorynchus (3) Tylenchus (2)

* Weinland Park Hough * * *

* *

* Weinland Park Hough

* *

a * * Weinland Park Weinland Park * *b Hough Hough

*d e *f *

Weinland Park Hough

* * *

Figure 3.2 Nematode community indices including enrichment index (EI), structure index (SI), channel index (CI), maturity index (MI), plant parasitic index (PPI), combined maturity index (CMI), Menhinic’s richness index, Shannon's diversity index, and evenness index in vacant lots in Weinland Park (Columbus) and Hough (Cleveland) neighborhoods (Ohio, USA). Data presented are Mean (± SEM), asterisks on the pair of bars indicate significant differences between the two neighborhoods at P ≤ 0.05

Risk Assessment for soil invertebrates

Comparison of vacant lot heavy metal concentrations to the USEPA Eco

SSLs for the metals showed that none of the vacant lots in either neighborhood had Pb or Cd concentration higher than SSLs of 1700 mg/kg and 140 mg/kg soil, respectively. However, all of the studied sites in both Weinland Park and Hough neighborhood had at-least one soil sample that exceeded the 120 mg/kg SSL for

Zn. There are no established SSLs for As and Cr contamination in soil.

Relationship between nematode community and heavy metals in Weinland Park

Neighborhood

The PCA was performed by dividing the nematode data into three groups of non-overlapping response variables: (i) nematodes grouped on the basis of their colonizer-persister scale (c-p scales 1 to 5); (ii) nematodes grouped on the basis of their feeding habit, i.e. bacteria feeding, fungus feeding, plant parasitic, predator and omnivores; and (iii) nematode community indices consisting of MI, PPI, EI,

SI, CI, Menhinic richness index, Shannon’s diversity index, and evenness index.

The PCA of environmental variables with the nematode c-p scales revealed clustering between c-p 1, 2 and 3 and soil active carbon content, whereas c-p 4 and 5 were strongly correlated with soil pH and As concentration (Figure 3.3 a).

The first and second components explained 35% of the variability in the data set.

When nematodes were grouped based on the different feeding habits, the first two components explained 37% of data variability (Figure 3.3 b). Bacteria and fungus

Figure 3.3 a Figure 3.3 b

Figure 3.3 c

71 feeding nematodes grouped with active carbon content, while predatory and omnivorous nematodes did not associate with any of the environmental variables.

Soil Cd, Cr, Pb and Zn had maximum contribution towards the first component and % clay, % silt, soil moisture and organic matter had maximum contribution towards the second component in both the above mentioned cases. The PCA of environmental variables with nematode community indices (Figure 3.3 c) showed that SI grouped with the heavy metals whereas EI and ratio of non-plant parasitic to plant parasitic nematodes were strongly correlated with soil moisture and % sand content. The first two components explained 37 % of data variability. Soil

Cd, Pb, Menhinic’s richness index and Shannon’s diversity index had the maximum contribution towards the first component and soil Cd, EI, CI and evenness index contributed towards the second component. Maturity index had an equal contribution towards both components.

The results of multiple regression analysis performed for the Weinland

Park neighborhood are provided in Table 3.3. A combination of % sand and active carbon content were found to be significantly correlated with the abundance of fungus feeding nematodes, while Cd and Zn concentrations along with soil pH were correlated with CI in the Weinland park neighborhood. Scatter plots for the lower trophic guild bacteria and fungus feeding nematodes with heavy metals (Figure 3.4) resulted in negative correlation with all the heavy metals except for a weak positive slope for fungus feeding nematodes with soil Pb concentration.

Response Predictor R-sq (adj) for Regression variable variable F P the model slope FF % sand 6.48 0.01 26.77 negative Active C positive CI Cd 4.25 0.00 25.54 negative Zn negative pH positive

(3.4 a) Weinland Park neighborhood (Columbus) Ohio

(3.4 b) Weinland Park neighborhood (Columbus) Ohio

Figure 3.4 Regression slopes for the lower trophic level bacteria and fungus feeding nematodes versus As, Cd, Cr, Pb and Zn conentrations (mg/kg soil) in Weinland Park neighborhood in Columbus, Ohio

Relationship between nematode community and heavy metals in Hough

Neighborhood

The PCA of environmental variables with nematode c-p groupings (Figure

3.5 a) showed c-p 3 nematodes correlated strongly with organic matter and active carbon content. C-p 5 grouped with % clay content and soil pH - while being equidistant from soil Cd, Zn, Cr concentrations and % silt. Soil Cr, % silt, % sand and organic matter content were the major contributors towards the first component while nematodes from c-p 1, 2, soil As and Pb contents were the major contributors towards the second component. The first two components explained 40% of the data variability. Figure 3.5 b shows the ordination diagram of environmental variables with the nematode feeding groups. Predatory nematodes grouped with soil As, moisture and % clay whereas the omnivores were associated with soil Cd, active carbon and organic matter. Bacteria and fungus feeding nematodes were separate from the rest of the environmental variables. The first two components explained 41% of data variability with soil

Cr, Zn, organic matter and % sand being the significant contributors for the first component and % clay, bacteria and fungus feeding nematodes were important contributors to the second component. Finally, PCA with the nematode indices

(Figure 3.5 c) showed that SI was strongly associated with soil As, Cr, pH, active carbon, organic matter and % silt content. The ratio of non-plant-parasitic to plant-parasitic nematodes was grouped in close association with % sand content.

Figure 3.5 a Figure 3.5 b

Figure 3.5 c

The first two components explained 36% of the data variability. Soil Cr, % sand,

% silt and organic matter content were the significant contributors for the first component and MI, EI, CI and Shannon’s diversity index were the important contributors for the second component.

Multiple regression analysis provided significant predictor variables explaining total abundance of nematodes, number of genera, nematodes belonging to c-p scales 1, 3 and 4, plant parasitic, bacteria feeding, fungus feeding, CI,

Menhinic richness index and evenness index (Table 3.4). The scatter plots of bacteria feeding nematodes with soil As showed a negative correlations, while Cr,

Pb and Zn gave a positive correlation. There was no discernible relationship with

Cd (Figure 3.6). Similarly the fungus feeding nematodes were negative correlated with soil As and positively with Cr and Zn, with no discernible relationship with

Cd or Pb. Scatter plots of the sensitive, omnivorous genera Eudorylaimus versus soil heavy metal concentrations showed a general trend of decreasing abundance with increasing soil metal concentration in Weinland Park neighborhood (Figure

3.7a); whereas in the Hough neighborhood, Eudorylaimus abundance was negatively correlated to As, and positively with Cd, Cr, Zn and Pb (Figure 3.7b).

Discussion

Soil is a vital resource for sustenance of life; however, its health and quality may be severely impacted by anthropogenic activities (Kabata-Pendias

Response Predictor R-sq (adj) for the Regression variable variable F P model slope Total N As 8.75 0.001 29.73 negative Cd positive Org matter positive Genera Cr 3.50 0.010 15.38 positive % silt positive pH negative Org matter negative c -p 1 pH 5.54 0.006 14.19 positive Org matter positive c -p 3 % silt 12.83 0.001 30.09 positive Org matter positive c -p 4 As 4.07 0.020 10.04 negative Cr positive FLN As 7.17 0.001 25.2 negative Cd positive Org matter positive PPN Cr 15.20 0.001 44.2 positive % silt positive Active C positive BF As 5.07 0.003 18.17 negative Cd positive Org matter positive FF As 8.98 0.001 30.33 negative Cd positive Org matter positive CI As 4.28 0.018 10.68 negative Cd positive Menhinic pH 13.27 0.001 30.86 negative Org matter negative Shannon % sand 3.50 0.030 8.42 positive % silt positive

78 Continued Table 3.4 continued

Evenness Cr 3.80 0.008 17.03 negative % silt negative pH positive Org matter positive

(3.6 a) Hough neighborhood (Cleveland) Ohio

(3.6 b) Hough neighborhood (Cleveland) Ohio

Figure 3.6 Regression slopes for the lower trophic level bacteria and fungus feeding nematodes versus As, Cd, Cr, Pb and Zn conentrations (mg/kg soil) in Hough neighborhood, Cleveland, Ohio

(3.7 a) Weinland Park neighborhood (Columbus) Ohio

(3.7 b) Hough neighborhood (Cleveland) Ohio

Figure 3.7 Regression slopes for Eudorylaimus versus As, Cd, Cr, Pb and Zn conentrations (mg/kg soil) in Weinland Park (Columbus, Ohio) and Hough (Cleveland, Ohio) neighborhoods

2000; Oldeman 1994). Intensive industrialization and increasing urbanization have decreased the quantity and quality of available agricultural land (Alphan

2003). Excessive soil disturbance, compaction, contamination, large scale soil erosion and nutrient losses are some of the negative effects of human activities that have resulted in soil degradation and a decline in food productivity in many regions (Alphan 2003; Oldeman 1994). Soil health is governed by the interaction of physical, chemical and biological components of the soil (Knight et al., 2013;

Reeves et al., 2013) and many soil dwelling organisms have been studied as bioindicators of soil health in industrial, agricultural and forest soils. Studies have used protozoans (Foissner 1999), invertebrates like earthworms, mites, springtails

(Paoletti et al. 1991; Paoletti et al. 1999), micro- and macro-arthropods (Van-

Straalen 1998), ants (Anderson et al. 2002; Lobry-De-Bruyn 1999) and soil bacteria and fungal communities (Schloter et al. 2003) as bioindicators. For this study we used the soil nematode community as an indicator of soil food web health in urban residential neighborhoods containing varying levels of heavy metal contamination. Nematodes spend their entire lifecycle in close association with soil particles and their abundance and diversity in a given ecosystem is governed by a variety of biotic and abiotic factors, their interactions (Yeates

1979), and the presence or absence of soil pollutants (Ekschmitt and Korthals

2006). Also, for the small, isolated urban vacant land parcels, the study of a single, more mobile species may not provide the desired level of sensitivity or specificity to environmental changes as would be displayed in the response of the

82 relatively less-mobile nematode community (Schloter et al. 2003; Van-Straalen

1998), making it an appropriate urban soil health indicator.

In a disturbed ecosystem, bacteria feeding nematodes are the predominant functional group, followed by plant parasitic nematodes (Yeates and Bongers

1999) as was observed in the vacant lots in both neighborhoods in this study. The

Hough neighborhood had a greater abundance of both bacteria and fungus feeding nematodes and higher PPI and CI, as compared to the Weinland Park neighborhood, which had higher EI, SI and nematode species richness. Both neighborhoods had very few nematodes belonging to k-selected guilds representing higher trophic level omnivorous or predatory nematodes (c-p scales 4 and 5). This may be attributed to the general disturbed nature of soil profile in urban ecosystems, as also noted in our previous studies (Park et al. 2010; Grewal et al., 2011; Knight et al. 2013). Additionally, heavy metal concentrations exceeding natural background levels found in Ohio (Sharma et al. 2014, in press) may also negatively impact the sensitive higher trophic level nematode groups

(Ekschmitt and Korthals 2006; Bardgett et al. 1994). Soil concentrations of As,

Cd, Cr and Zn were higher in Weinland Park neighborhood whereas Pb was higher in the Hough neighborhood (Sharma et al. 2014, in press). Furthermore, overall nematode abundance in Weinland Park neighborhood was lower than

Hough, which may suggest that some interaction between soil environmental parameters in the two neighborhoods with their respective heavy metal concentrations and their influence on the soil food web.

Comparison of the vacant lot heavy metal concentrations with the

Ecological SSLs of the heavy metals for soil invertebrates provided an estimate of the potential risk of metals to the soil food web. All of the vacant lots in Weinland

Park and Hough neighborhoods had at least one soil sample with Zn concentration exceeding the Eco SSL value of 120 mg/kg soil. This value was derived from studies analyzing the effect Zn on springtails and nematodes. However all of the studies used by the EPA were conducted in acidic soil with pH < 5 and organic matter content less than 4%. Vacant lots in Weinland Park and Hough neighborhood had neutral soil with an average pH value of 7.5 and 7 respectively, along with the average organic matter content > 4%, ranging upto a maximum of

7% in Hough and 14% in Weinland Park. Therefore, Zn is expected to be less soluble in soil and strongly adsorbed to organic matter in these neutral conditions

(USEPA, 2007). Additionally, it was not a significant factor in the regression analysis with any of the nematode community parameters further indicating the absence of Zn toxicity in the vacant lots. Although our previous study (Chapter 2) indicated that approximately 86% (13 out of 15) of the lots in Weinland Park and

89% (25 out of 28) of the lots in Hough neighborhood had Zn concentrations higher than natural background concentrations in Franklin and Cuyahoga counties, we do not see any indication of its toxicity to humans (Chapter 1) or to soil invertebrates when compared to the USEPA SSL. However, the lower trophic groups of bacteria and fungus feeding nematodes showed negative associations with Zn concentration in Weinland Park neighborhood. This suggests the need of

84 further research for a clearer understanding of the effect of Zn on different nematode trophic levels representing the complete soil food web and their ecosystem services potential in the urban soil ecosystem.

Soil Pb concentration in the vacant lots in both neighborhoods was below the SSL of 1700 mg/kg soil (USEPA, 2005) for soil invertebrates and it was not a significant variable in any of the regression models with the nematode community parameters. Hence it may be an indication that Pb concentrations in these vacant lots may not pose any risk to soil invertebrates. However, the Eco SSL value of

1700 mg/kg soil has been derived by the EPA using studies only with collembolans as the test organism. This may not be an accurate representation of the entire soil food web with its multiple trophic levels consisting or species with different sensitivities to Pb. Additionally, all of the vacant lots in both neighborhoods had Pb concentration higher than the natural background concentrations in Franklin and Cuyahoga Counties (Chapter 2). About 6% (1 out of 15) of the lots in Weinland Park and 53% (15 out of 28) of the lots in Hough neighborhood also had Pb concentrations exceeding the SSLs for potential human risk i.e., 400 mg/kg soil (Chapter 2). Also Pb concentrations showed significant correlations with most of the measured soil properties. Hence, the elevated Pb concentration in both neighborhoods in conjunction with the soil properties may have some interactions with the soil nematode community contributing to its lack of structure. For example, Pb concentration in Weinland Park had a negative association with the higher trophic level nematode Eudorylaimus. Therefore, the

85 influence of Pb concentrations on the soil food web, specifically on higher trophic levels needs to be further explored.

Ecological SSL of 140 mg Cd/kg soil was higher than the Cd concentrations observed in all the vacant lots in both neighborhoods, which were within natural background concentrations. Hence the vacant lots may be considered safe for soil invertebrates with respect to Cd concentrations.

Nevertheless, this value was derived from studies using springtails, earthworms and a single lower trophic level nematode species as test organisms. Hence again this may not be an accurate representation of the complexity of the below ground soil food web. Also, Cd showed correlation with CI in Weinland Park neighborhood and the total nematode abundance, abundance of bacteria and fungus feeding nematodes and CI in the Hough neighborhood in the multiple regression analysis. It is also important to note that regression models with Cd as an important contributing factor also always had soil As concentration and organic matter present along with Cd. Hence, it may not be just the Cd metal concentration, but its co-relation with other metals and organic matter that may be interacting with the nematode trophic groups contributing to the variation in the abundance of the different trophic guilds.

The USEPA has not provided any Eco SSL values for As or Cr contamination in soil due to lack of sufficient number of studies. This study could shed some light on As and Cr interaction with respect to the soil nematode community. We acknowledge that both of these metals were not elevated in the

86 vacant lots in both neighborhoods. Hough neighborhood (Cuyahoga County) and

Weinland Park neighborhood (Franklin County) have naturally elevated soil As concentrations due to the bedrock which comprises of old shale deposits (Venteris et al. 2014). Also, the presence of these two metals as important factors in the multiple regression analysis is probably an artifact of their significant correlations with other soil properties such as organic matter, soil texture and pH (Chapter 2).

However, the biological significance of the negative association of soil As with bacteria and fungus feeding nematodes and the higher trophic level Eudorylaimus nematode species in both neighborhoods warrants further empirical investigation of the interactions of As with the nematode community. Similarly, negative associations of soil Cr with bacteria and fungus feeding nematodes and

Eudorylaimus in Weinland Park neighborhood also need to be further explored. A possible explanation could be that higher concentrations of these metals suppress nematode abundance; however at lower concentrations interactions with other soil properties govern nematode densities.

In the Weinland Park neighborhood, fungus feeding nematodes were an important indicator guild showing significant interactions with the environmental parameters. Their abundance was positively correlated with the soil active carbon content and negatively with % sand content. Also variation in CI, which indicates the relative involvement of fungus feeding nematodes in the flow of carbon and energy through the soil food web (Ferris et al. 2001), was significantly associated with a combination of multiple environmental variables. It was negatively

87 correlated with soil Cd and Zn concentrations and positively with soil pH.

Doelman et al. (1984) showed that the synergistic effect of multiple metal solutions on the rate of reproduction of bacteria feeding nematode, Mesorhabditus monhystera and fungus feeding nematode, Aphelenchus avenae, led to a greater decrease in their reproduction as opposed to the effect of individual heavy metal solutions. Also, the mixed metal solutions resulted in a more severe impact on population size and toxicity at lower metal concentrations in the fungus feeding species. Our results with negative associations of the lower trophic groups with the individual metals in Weinland Park (Figure 3.4) and negative correlations in the multiple regression analysis (Table 3.3) may indicate potential toxicity due to synergistic effects of Cd and Zn on the lower trophic group bacteria and fungus feeding nematodes in urban soil. Heavy metals can also inhibit growth of bacteria and fungi directly thereby diminishing the nematode food sources and reducing their densities (Doelman et al. 1984). This shows that in the absence of more sensitive higher trophic level nematodes, the abundance of fungus feeding nematodes and CI may serve as indicators of the soil food web health (Yeates and

Bongers 1999).

Principal component analysis showed that the interactions between the soil metal concentrations and the nematode food web may be affected by significant correlations between the metals and soil properties. A strong clustering of all metals along with soil pH, positive association with organic matter and negative with clay content indicates the influence of these soil properties on the bio-

88 availability and solubility of these metals in soil (USEPA 2005, 2007; Adriano

2001; Kabata-Pendias 2000; Anderson et al. 1988). A greater clay fraction in soil with neutral pH and high organic matter content, as observed in the Weinland

Park, would stabilize/bind the metals to the functional groups of organic matter and clay particles in soil (Adriano 2001; Kabata-Pendias 2000; Anderson et al.

1988).

In the Hough neighborhood, soil texture, organic matter, As and Cd concentrations were important environmental parameters associated with the nematode community. Soil As and Cd concentration showed an intrinsic relationship as they were generally found together as significant factors associated with most of the nematode response variables, with As showing a negative association and Cd with a positive association. Additionally, in the principal component analysis, As was not closely associated with the other metals, indicating a unique relationship of As with the nematode community. Also, soil texture, pH and organic matter content can affect the bioavailability of metals in soil (Adriano 2001; Kabata-Pendias 2000; Yeates and Bongers 1999). Sandy soil texture and low organic matter content (mean = 4.3%) in Hough neighborhood as compared to the clayey texture and higher organic matter (mean = 6.7%) in

Weinland Park neighborhood (Chapter 2) may result in higher As availability in the Hough neighborhood soil, which in association with other soil properties may be an important factor contributing to the loss of structural complexity in the urban soil food web. Soil As concentrations may negatively affect the bacteria

89 and fungus feeding nematodes directly through enzyme toxicity or through association of the metal with bacteria and fungi consumed as food source (Lorenz et al. 2006; Doelman et al. 1984). This may also highlight the importance of lower trophic level bacteria and fungus feeding nematodes as indicators of metal stress to soil, similar to the findings of Pen-Mouratov et al. (2007) who observed correlations between metals and bacteria-feeding nematodes in an industrial site.

Soil Cd concentrations in the Hough neighborhood was significantly lower than that observed in the Weinland Park neighborhood (Chapter 2). Positive associations of total abundance, abundance of bacterial and fungal feeding nematodes with Cd may be explained as nematodes being relatively insensitive to low soil Cd concentrations (Kammenga et al. 1994) or the positive correlation may be a result of interaction with other environmental variables such as weak associations with organic matter (Anderson et al. 1988) which also had a positive correlation with most of the nematode community parameters. Hence the negative correlation with As and positive with Cd, may be a characteristic relationship shown by the two metals with the lower trophic level bacteria feeding and fungus feeding nematodes in the Hough neighborhood. This was contrary to the findings of Bardgett et al. (1994) who did not see any such relationship between metals and bacteria feeding nematodes in their study.

A similar pattern of negative correlation with As and positive with soil Cr concentrations was also observed with nematodes belonging to c-p scale 4 in their regression slopes with the individual heavy metals and in the PCA ordination

90 diagrams. Plant parasitic nematodes also showed a positive correlation with Cr, % silt and soil carbon content. Chromium is essential in the functioning of several enzymes in soil microrganisms and plants and hence its presence in low concentrations may have increased microbial and plant growth, thereby stimulating growth of bacteria feeding and plant parasitic nematodes through tritrophic effects (Bakonyi et al. 2003). Organic matter and active carbon content was also important factors in the regression model with abundance of nematodes belonging to c-p scales 1 and 3, richness index, and evenness index, indicating the importance of nutrient enriched soil for a greater abundance of lower trophic level nematodes (Ferris and Bongers 2006, Yeates and Bongers 1999). Shannon's diversity index, total number of genera and plant parasitic nematodes showed significant positive association with % silt and % clay content in soil, and a significant negative association with % sand. This shows that nematodes may prefer clayey to silty soils and that texture plays an important role in determining the soil food web diversity and species richness (Yeates and Bongers 1999).

Out of all the higher trophic level omnivorous and predatory genera observed in all the samples from both neighborhoods, Eudorylaimus was found in the highest proportion of samples (45%) in Weinland Park neighborhood and

Hough neighborhood (55%). While the samples in Weinland Park showed a clear negative association of Eudorylaimus abundance with increasing heavy metals concentrations (Figure 3.7 a); in the Hough neighborhood, soil As concentrations had a negative slope, while Cd, Cr, Pb and Zn had weak positive slopes (Figure

3.7 b). Higher concentrations of heavy metals in association with other forms of soil disturbance such as soil mixing and excavation may have contributed to the negative trend lines in Weinland Park, indicating the potential harmful effects of disturbance to the more sensitive higher trophic guilds in the urban soil food web.

While it has been shown that greater soil heavy metal concentrations can suppress abundance of higher trophic level nematodes (Zullini et al. 1985; Pen-Mouratov et al. 2008), the variation in nematode population at low metal concentrations should be further explored. Although the results from both neighborhoods were not statistically significant, their biological relevance is important in understanding the negative influence of soil disturbance, compaction and heavy metal concentrations on soil food web complexity.

Overall, the principal component analysis produced different clustering of variables in the two neighborhoods. The contribution of the first two principal components in explaining data variability ranged from 35% to 41% in the individual neighborhood analyses. We also combined the data sets from the two neighborhoods to obtain a larger range of values for the soil parameters and metal concentrations to explore if similar relationships existed between the nematode and environmental parameters. However, combining the data sets resulted in dissimilar clustering of variables in the PCA ordination charts and the correlations observed between the environmental and nematode community variables were different from the correlations in the individual neighborhood analysis (data not shown). Hence, these results are specific to the two communities and should

92 ideally not be extended to a different location. They are specific to the soil texture, moisture, pH, organic matter, active carbon content and nematode community observed in the Hough and Weinland Park neighborhoods. The results should not be extended to other sites and locations varying in soil texture, moisture, plant cover, organic matter content, etc., should not be analyzed together when establishing a food garden. This can negatively impact the management approach employed by the neighborhood's food production program, such as the rate and time of application of organic amendments or other management practices for crop production.

In conclusion, we tried to fill a major gap in knowledge on the associations between soil properties, metal concentrations and the health of soil food webs in urban vacant lots slated for urban agriculture through this study. We explored if the heavy metal concentrations were of any potential risk to soil invertebrates based on USEPA Eco SSLs for the different metals. Only Zn was established as a metal of concern for the soil nematodes in comparison to the Eco

SSL value of 120 mg/kg soil, however the test organism used in most studies may not have provided a representation of the complexity and structure of the below ground soil food web. Furthermore, other metals such as As, Cd and Cr, in association with soil properties could influence population dynamics within the nematode community. Hence these associations need to be further explored across a larger number of sites varying in their metal concentrations and soil properties to further understand the influence of metal concentrations on the urban soil food

93 web. Soil physical, chemical and biological compositions differ spatially in the studied urban ecosystems and are impacted by ongoing anthropogenic activities.

Based on our analysis we predict that a combination of these parameters along with the metal concentrations is responsible for the observed lack of structure and complexity in the urban soil food web. This can severely limit their ecosystem services potential such as nutrient cycling, organic matter decomposition and biological pest and disease regulation and be a detriment to urban agriculture.

Acknowledgements

We thank the Cleveland Planning Commission and the Hough neighborhood Land Bank for help with identification of city owned lots in

Cleveland for sampling, and the Weinland Park Neighborhood Association, Mid

Ohio Regional planning Commission and Wagenbrenner Corporation for permission to sample vacant lots in the Weinland Park Neighborhood in

Columbus. We also thank the U.S Department of Housing and Urban

Development along with the Urban Landscape Ecology Program, the Center for

Urban Environment and Economic Development, the Food Innovation Center

Grant, and the OARDC Competitive Research Grants Program for funding. We acknowledge the help from Mr. Kevin Power and Priyanka Yadav of the Urban

Landscape Ecology Program at the Ohio State University for assistance with sampling.

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Chapter 4: A novel approach to restoring structural complexity in soil food

webs

Abstract

Soil food webs provide ecosystem services that form the basis of sustainability in all terrestrial biomes. However, in urban and agroecosystems the soil food webs are often degraded, short and dominated by opportunists at the entry level. In this study, we show how the structural diversity of the soil food web can be restored using nematode community as a bioindicator taxon. As nematodes occur at multiple trophic levels within the soil food web, we hypothesized that the missing trophic guilds (along with their associated suite of organisms) can be re-established in a disturbed ecosystem by transplanting small intact soil cores. The results showed that opportunistic bacteria feeding (BF) and fungus feeding (FF) nematodes moved out of the transplanted cores and colonized a 60 cm X 60 cm arena containing autoclaved soil within 2 weeks, and the higher trophic level omnivorous (OM) and predatory (PR) nematodes began to spread out into the arena by week 5. Field trials in turf grass plots lacking the nematode higher trophic guilds supported our hypothesis and showed a significant

100 colonization of the plots by the OM and PR nematodes exiting the forest soil cores, resulting in increases in structure index (SI) and maturity index (MI) of the soil food webs compared to plots receiving no core transplants or those receiving commercial topsoil application. The soil food web restoration potential of the core transplants with or without organic amendments varying in C:N ratios was then evaluated in urban vacant lots containing a low level of heavy metal contamination. Results revealed that organic compost with a C:N ratio of 12:1 resulted in maximum increase in the abundance of higher trophic level nematodes and the SI and MI of the soil food web, as compared to the use of grass clipping

(C:N = 20:1) or organic peat (C:N = 25:1). Application of only organic amendments did not introduce any of the missing higher nematode trophic guilds into the soil ecology. It is concluded that the use of small intact soil cores from nearby undisturbed forest areas along with an organic amendment with low C:N ratio can restore soil food web complexity by re-establishing the missing trophic links as opposed to the application of only organic amendments or using topsoil.

This study provides a new approach for restoring the functional complexity of soil food webs, improving their potential to provide essential ecosystem services. The new approach is less destructive to the contributing ecosystem and would be more cost-effective than a complete replacement of topsoil that is commonly practiced in cities at this time.

101

Introduction

Sustainable production of healthy food and other ecosystem services for the expected population of 9 billion people (Godfray et al., 2010) without further harm to the environment is one of society’s grand global challenges. A structurally diverse soil food web enables sustainable food production along with a suite of other ecosystem services such as cycling of nutrients and minerals, organic matter decomposition, regulation of pests, pathogens and weeds and increased plant biomass (Doran and Zeiss, 2000; Brown and Tworkoski, 2004;

Brussaard et al., 2007; Pretty, 2008; Scherr and McNeely, 2008; Yadav et al.,

2013). However, these soil food webs have been degraded due to increased human activity and now tend to be short and dominated by opportunists at the entry level in many ecosystems (Duffy et al., 2007; Ferris and Matute 2003; Briar et al., 2007; Grewal et al., 2010). Restoration of soil food web structural complexity is critical to regain functional diversity and to ensure sustainability of the vital ecosystem services. Greater species and functional diversity, and more importantly response diversity (Elmqvist et al., 2003) in the soil food webs allows for increased resilience against external shocks such as biological invasions and environmental disturbances (Hedlund et al., 2004; Brussaards et al., 2007), enabling recovery of ecosystems from stress and preventing regime shifts.

Soil food webs in agricultural ecosystems are particularly degraded due to a multitude of frequent disturbances including tillage, seeding, harvesting, and fertilizer and pesticide applications (Childe, 2013; Brussaards et al., 2007; Tilman

102 et al., 2002; Briar et al., 2007a) and agricultural productivity has declined in several parts of the world (Millennium Ecosystem Assessment 2005; Liu et al.

2007; Doran and Zeiss 2000). Even in organic farming systems intensive tillage and mechanical weed control practices destroy soil food web structural complexity (Briar et al., 2007) despite the use of cover crops, thus eliminating services provided by the tillage-sensitive higher trophic level species. Tillage and other agricultural practices affect soil food webs directly through repeated physical damage to invertebrates, fungal hyphae, and mycorrhizal associations.

Tillage also indirectly affects soil food webs by exposing organisms to lethal ultra violet radiation, increasing soil aeration and temperature, accelerating soil organic matter decomposition, exposing protected C, N, and P to microbes, promoting bacterial dominance, and reducing biodiversity (Hendrix et al., 1986; Angers et al., 1993; Frey et al., 1999, Lundquist et al., 1999; Kalbtz et al., 2002, Briar et al.,

2007, 2011; Carmen et al., 2010; Groenigen et al., 2010).

Although information from urban ecosystems is limited, recent studies point to trophic downgrading even in urban soil food webs. Studies have revealed that nematode food webs in urban soils lack structural complexity and often contain few to no nematodes belonging to higher trophic level predatory and omnivorous species (Briar et al., 2007a; Pavao-Zuckerman and Coleman, 2007;

Cheng and Grewal, 2008; 2009; Grewal et al., 2010; Park et al., 2010). At the same time, interest in urban agriculture is rising because urban food production can bring about a significant change in the diet of low income residential

103 neighborhoods through the provision of nutritious, low cost fruits and vegetables locally (De Bon et al., 2008). Furthermore, cities, especially those with declining populations, have been predicted to possess substantial potential to become self- reliant in fresh produce (Grewal and Grewal, 2012) by reclaiming the accumulating vacant land. However, poor soil quality (1991De Kimpe and

Morel, 2000; Jim, 1998; Pouyat and McDonnell) and contamination (Sharma et al., 2014; McClintock, 2012) prevent the use of readily available urban vacant land for sustainable food production in cities.

Three distinct methods are currently employed to improve degraded soils, although none focuses specifically on the restoration of soil food web complexity.

One method involves the addition of organic matter to soil in the form of compost, manure or cover crop residues to improve the general nutritional, physical and biological condition of the soil, and is more commonly practiced in agroecosystems (Cooger, 2005; Bulluck et al., 2002). Such organic amendments can enhance the functioning of the soil food web by affecting the growth and responses of the resident microbial fauna (Ferris and Matute 2003) however they are rarely used for adding novel microbial or invertebrate communities to the soil.

More importantly these organic amendments do not restore soil food web structural complexity (Cheng and Grewal, 2008). Also opportunities for re- colonization are limited for less mobile soil fauna, especially in fragmented urban landscapes (Bryant, 2006; Mckinney, 2002; Wang and Moskovite, 2002; Byrne and Grewal, 2009). The second method involves the inoculation of specific

104 microbes to the soil to enhance specific plant mycorrhizal or rhizobial associations and improve plant health (Jeffries et al., 2003; Vessey, 2003) or the application of biocontrol agents such as bacteria, fungi or nematodes to control specific target pests and plant pathogens (Grewal et al., 2005; Butt et al., 2001;

Guetsky et al., 2001). The third method involves a complete replacement of topsoil with soil brought from other areas and is more commonly employed in urban ecosystems. However, during the process of soil excavation, transportation and storage, often on concrete driveways or parking lots, no attention is paid to the survival of meso- and micro-faunal communities, which can result in the loss of higher trophic level species that are more sensitive to such disturbances

(Bongers and Ferris, 1999). Disturbance also occurs during shoveling, mixing and preparation of raised beds for planting, further affecting the survival of the sensitive higher trophic guilds. Complete replacement of topsoil requires hauling large quantities of soil which is not only costly, but also contributes to disruption of ecological processes in both the contributing and recipient ecosystems.

As restoration of structural complexity of the soil food webs is essential to regain the full scope of their ecosystem services and to maintain ecosystem resilience, new approaches for soil food web reconstruction are needed. Here, we report on the development of one such new approach to restore the structural complexity in degraded soil food webs. Using nematode community as a surrogate for the soil food web and higher nematode trophic guilds as bioindicators, we assessed the possibility of restoring the structural complexity of

105 urban soil food web to levels observed in relatively undisturbed forest soils. We hypothesized that the missing soil nematode trophic guilds (along with their associated organisms) can be transferred and established in a disturbed ecosystem missing those guilds. The specific objectives of the study were to: (i) determine the feasibility of transferring the intact soil food web from a forest ecosystem using small soil cores into autoclaved soil in the laboratory; (ii) compare the effectiveness of soil core transplants to commercial topsoil application to reestablish the missing trophic links in the disturbed soil food webs in turfgrass plots; and (iii) examine the effect of organic amendments differing in C:N ratios on the survival and sustenance of the introduced higher trophic level nematodes in heavy metal contaminated urban vacant lots.

Materials and Methods

Effectiveness of soil core transplants for re-construction of the soil food web in autoclaved soil:

To test if intact soil food webs can be transferred using soil cores, wooden microcosms (60cm X 60cm X 5cm height) were filled with autoclaved soil collected from a community garden in the Weinland Park neighborhood in

Columbus, Ohio. Intact soil cores were removed from the Gross-Jean Farm woodlot in Wooster, Ohio using a golf-course cup-cutter (9 cm diameter, 5 cm deep) and transported to the lab in a cooler carefully to minimize disturbance.

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One such core was transplanted in the center of each microcosm and four such microcosms were prepared. All microcosms were carefully watered with a sprinkling can avoiding flooding and covered with black plastic sheet to minimize evaporation. Soil samples were collected at 5, 10, 15, and 20 cm distance from the edge of the transplanted core, using a soil corer (2 cm dia, 5 cm height) for nematode community analysis. Holes created due to sampling were filled with sterile top soil to avoid disruption in the nematode movement and a different transect was selected for sampling each week. Microcosms were placed in the lab at room temperature (~22oC) and sampling was done weekly for 5 weeks.

Comparison of forest soil cores and commercial topsoil for re-establishing missing trophic links in the disturbed soil food webs in turfgrass plots:

Baseline soil nematode food webs in the targeted turfgrass plots and the nearby forest habitat: Baseline data on nematode community structure in turf-type tall fescue (Festuca arundinacea) plots established on subsoil (see details below) and the Grossjean woodlot in Wooster, Ohio was collected in July 2013 using a soil corer (3cm dia by 10 cm deep). Five random samples were collected from each of the ten turfgrass plots and composited by plot in labelled plastic bags.

Three random 50 m by 50 m areas were selected in the GrossJean woodlot and ten soil cores (3 cm dia by 10 cm deep) were collected from each area, at-least 5m apart, and mixed together to form a composite sample each area. The samples

107 were transported to the lab in coolers and a 10 g subsample was used for nematode community analysis (see below).

Experimental design and treatments: The effectiveness of soil core transplants was compared with standard commercial topsoil application in turf- type tall fescue plots established on subsoil at the Ohio State University campus in Wooster, Ohio. The plots were established in 2006 and the detailed description of the establishment procedure is given in Cheng and Grewal (2009). The plots had since been maintained by fortnightly mowing, during the growing season, at the height of about 10 cm and no organic amendments, fertilizers or pesticides had been applied until the start of this experiment. Each plot was 1.5m X 2m, surrounded by wooden boards and separated by a 2.5m buffer area to prevent plot to plot contamination. In August 2013, five plots were randomly selected to receive one of the two treatments: the forest soil core or commercial topsoil application. For the soil-core transplant treatment, a 9cm dia and 10cm deep soil core was removed using a golf-course cup-cutter from the center of each sub-plot and replaced with the same size intact forest soil core brought from the GrossJean

Woodlot. For the commercial topsoil application treatment, an equivalent volume

(as the forest soil core ~ 636 cm3) of commercial topsoil was uniformly spread on the surface of the five plots by hand. The commercial topsoil (Earthgro, Scotts

Miracle-Gro, Scotts Company LLC) purchased from local gardening stores in

Wooster, was placed in a heap on a concrete floor in a greenhouse at 28oC for 3

108 days to mimic conditions typically experienced when topsoil is transferred in large quantities for gardening or other landscaping purposes.

Data collection: Changes in the nematode community in plots were determined by taking soil samples from each plot along a transect at 15 cm, 30 cm and 45 cm distances from the center of each plot (or edge of the transplanted core). Sampling was continued weekly for the first four weeks, and every two weeks thereafter till week 8. The field trial was carried out from August through

October, with average soil temperature ranging from a high of 23.9oC in August to a low of 12.1oC in October (OARDC, Wooster Weather Station). The plots were lightly watered using a hose as needed and mowed weekly to a grass height of 7.6 cm for the duration of the study.

Effectiveness of soil core transplants with or without organic amendments in urban vacant lots:

Baseline soil nematode food webs in the targeted vacant lots and the nearby forest habitat: Baseline data on nematode community structure in two urban vacant lots in the Weinland Park neighborhood in Columbus, Ohio (see details below) and a woodlot at the Waterman Agricultural and Natural Resource

Laboratory located on the Ohio State University campus in Columbus, Ohio was collected in July 2013 using a soil corer (3 cm dia by 10 cm deep). Nine random samples were collected from each lot and composited by lot in labelled plastic bags. Three random, 50 m by 50 m, areas were selected in the Waterman woodlot

109 and ten soil cores (3 cm dia by 10 cm deep) were collected, at-least 5 m apart, and mixed together to form a composite sample per area. The samples were transported to the lab in coolers and a 10 g subsample was used for a comprehensive nematode community analysis (see below).

Baseline soil chemical analysis in the targeted vacant lots and the nearby forest habitat: Concentrations of As, Cd, Cr, Pb and Zn (mg/kg soil) were determined for vacant lot samples and the forest soil sample prior to setting up the experiment using EPA method 3051A. Soil pH was determined using a glass electrode in a 1:1 soil and deionized water mixtures. Antecedent soil moisture content was measured and particle size analysis to determine the relative proportions of sand, silt and clay. Detailed description of the method is provided in Sharma et al. (2014).

Experimental design and treatments: To evaluate the effect of organic matter amendments on the effectiveness of the core transplant method in reconstruction of the soil food web in urban soil, we selected two adjacent vacant lots (lot A towards north and lot B towards south) that had a low level of heavy metal contamination based on our previous study (Sharma et al., 2014) in the

Weinland Park neighborhood (30.987488, -83.000598) in Columbus, Ohio. A description of the neighborhood is provided in Sharma et al. (2014). Both lots were roughly 12 m wide and 20 m long. Both lots were similar except that lot A had a small 4 m X 3 m vegetable garden at the northeast corner and lot B had some trees along its south edge. Both lots had almost complete grass cover with a

110 few weed species including Trifolium repens (white clover) and Taraxacum officinale (dandelion) and were mowed weekly to a height of about 7.6 cm.

On each vacant lot, 1.5 m X 1.5 m plots were demarcated with flags, separated from one another by 1.5 m wide buffer areas. The experiment was laid out as a randomized block design (RBD) with 3 blocks on each lot. The treatments were assigned randomly to plots and all amendments (see below) were top-dressed to a height of about 1 inch on the soil surface, one week prior to the core transplantation. There were five treatments: (i) forest soil core only; (ii) forest soil core + organic compost; (ii) forest soil core + organic peat; (iii) forest soil core + grass clippings; and (v) compost only. Organic matter amendments consisting of compost, grass clippings and peat were selected due to their varying

C:N ratios: 12:1, 20:1 and 25:1, respectively. The organic compost (Schultz

Premium Compost and Manure, Infinity Lawn and Garden Inc., Milan, IL) and peat (Organic Peat, Infinity Fertilizers Inc., Milan, IL) were purchased locally from a gardening store in Wooster, Ohio. The grass clippings were gathered by mowing the targeted vacant lots and dried in the sun on a parking lot for a day.

Approximately 2 kg (dry weight) of clippings was spread back on the assigned subplots by hand to cover the entire surface. The forest soil cores (~ 636 cm3) were collected using a golf-course cup-cutter (9 cm dia and 10 cm deep) from the

Waterman woodlot. The cores were transported to the site in a cooler carefully to avoid disturbance and one core was transplanted in the center of each plot after

111 removing the same size core from the plot. Plots were lightly irrigated as needed with a watering hose.

Data collection: To assess changes in the soil nematode community in the plots, 3 soil core samples were collected, using the 3 cm diameter soil corer to a depth of 10 cm, along a transect from each plot at distances of 15 cm, 30 cm and

45 cm from the edge of the forest soil core (or center of the plots without a core).

The individual core samples were placed in different, labeled polythene bags and transported to the laboratory in a cooler for nematode extraction and community analysis from all replicates giving a total of 90 samples each week (3 distances X

5 treatments X 3 blocks X 2 lots). Samples were taken weekly for the first 4 weeks, then once every two weeks till week 8 and finally in week 11.

Nematode Community analysis

For all the above experiments, nematodes were extracted using a 10 g subsample from each soil sample collected from each plot, using the Baermann funnel technique (Flegg and Hooper, 1970) at 22OC over a period of 72 hours.

The extracted nematodes were concentrated to a volume of about 5 ml and instantly heat killed at ~50oC. Nematodes were observed with the help of an inverted stereo microscope and a gridded petri plate where the first 100 were identified to the genus level using the ‘Interactive diagnostic key to plant parasitic, free-living and predaceous nematodes’ made available by the University of Nebraska Lincoln, Nematology Lab, based on original publication by Tarjan et

112 al. (1977). The remaining nematodes were counted to give the total number in each sample. A similar procedure was used to obtain the baseline nematode community data for the forest soil and organic compost and peat amendments.

Bongers, 1990; Ferris et al., 2001).

Statistical Analysis:

Nematode abundance data were transformed using the natural log transformation to meet the assumption of normality. Counts of PR and OM nematodes were arcsine transformed. Multivariate repeated measures analysis of variance (PROC GLM) was performed on the abundance data for nematodes and calculated community indices across the time period to compare differences over time and in the different treatments across the different distances using Wilk’s

Lambda F statistic (SAS Release 9.2, SAS Institute Inc., 2008). The means were

113 separated using Tukey’s test at P < 0.05. Comparisons were made between the initial nematode abundance data on the vacant lots and the final nematode abundance after 11 weeks using one way ANOVA. Since there were no statistical differences between the two vacant lots (data not shown), the nematode abundance data was lumped together and analyzed using SAS 9.2. Soil nutrient data from Oct 2013 was compared using one way ANOVA to look for differences between the 5 individual treatments in the urban vacant lot study using Minitab v.16 (Minitab, Inc, State College, PA).

Results

Effectiveness of soil core transplants for re-construction of the soil food web in autoclaved soil:

Nematode community moving out the forest soil cores and colonizing the surrounding autoclaved soil during the first two weeks was primarily composed of

BF nematode genera Rhabditis, Panagrolaimus, and Pelodera in the core transplanted microcosms. Figure 4.1 shows the abundance of nematodes classified on the basis of their feeding types at 5, 10, 15 and 20 cm distance from the edge of the transplanted forest soil core over the 5-week period. Overall, a multivariate repeated measures analysis with Wilk’s Lambda test showed that total abundance of nematodes was affected by time across all distances (F = 48.2; df = 4, 25; P < 0.001) and there was an interaction between time and distance (F =

114

Figure 4.1: Mean (± S.E.) total abundance and abundance of bacteria feeding, fungus feeding, plant parasitic, omnivorous and predatory nematodes in frames with the transplanted forest soil cores at 5, 10, 15 and 20 cm distances from the edge of the core, across the time period of 5 weeks. Letters over bars indicate significant difference between distances in individual week at P ≤ 0.05.

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3.17; df = 12, 66; P < 0.01). Total nematode abundance at 5 and 10 cm distances in week 1was significantly higher than that at 15 and 20 cm. In week 2, total nematode abundance at 10 cm was also greater than 5 and 15 cm, and there were no differences between distances during weeks 3 to 5 as the entire area in the microcosms was colonized by the nematode community moving out of the forest cores. Similarly, abundance of BF nematodes varied over time (F = 41.42; df = 4,

25; P < 0.001) and also showed interaction between time and distance of sampling from core edge (F = 2.95; df = 12, 66; P < 0.01). BF nematode abundance at 5 and 10 cm distances in week 1was significantly higher than that at 15 and 20 cm and it was greater at 10 cm than 5 and 15 cm. There were no significant differences in BF nematode abundance at different distances in weeks 3 to 5.

Fungus feeding nematodes belonging to genera Aphlenchus and Aphlenchoides slowly increased in abundance reaching peak populations in weeks 3, 4 and 5 with numbers ranging from 100 to 250 nematodes per sample. The variation in abundance showed a significant effect of time (F = 100.06; df = 4, 25; P < 0.001).

There was no overall interaction between time and distance of sampling except in week 4 where abundance at 15 cm was greater than 20 cm. Plant parasitic nematodes were found at much lower numbers, ranging from 2 to 15 per sample.

Their abundance did not show any significant effects of time or distance of sampling.

Predatory and omnivorous genera, Mononchus, Dorylaimus, and

Eudorylaimus ranged from 10 to 50 nematodes per sample. Predatory nematodes

116 had the highest abundance closest to the transplanted core and were significantly lower at 10, 15 and 20 cm distances. Their abundance showed an overall effect of time (F = 6.84; df = 4, 25; P < 0.001). There were significant differences in their abundance at different distances in weeks 2, 3 and 5 with abundance at 5 cm from the core being significantly higher than at other distances. By week 4, predatory nematodes had spread throughout the microcosm except that the 20 cm distance had the lowest abundance. Omnivore nematode abundance showed a significant effect of time (F = 44.59; df = 4, 25; P < 0.001) and interaction between time and distance (F = 2.5; df = 12, 66; P < 0.01). There were significant differences between the distances in weeks 2, 3, 4 and 5 with greater abundance closer to the core than further away.

Comparison of forest soil cores and commercial topsoil for re-establishing missing trophic links in the disturbed soil food webs in turfgrass plots:

The baseline nematode community in the Turfgrass plots was primarily made up of the opportunistic BF and PP nematodes, with BF comprising almost

70% of the total population. Plant parasitic nematodes made up 16% and FF about 10%, whereas PR and OM nematodes made up less than 3% of the total population. The more commonly found BF nematodes belonged to Cephalobus,

Panagrolaimus and Rhabditis genera, while Filenchus was the most common PP

117

Table 4.1: Mean abundance and standard error of mean (SEM) for total numbers of nematodes and genera and nematode genera belonging to different trophic groups along with the calculated community indices from soil samples (10 g each) collected from GrossJean forest woodlot and the turfgrass plots in Wooster, Ohio.

GrossJean woodlot Turfgrass plots Trophic guilds/indices Nematode genus Mean SEM Mean SEM Bacteria Feeding Acrobeles 16.5 0.4 Acrobeloides 15.2 0.5 12.2 0.6 Alaimus 4.0 0.1 1.6 0.3 Cephalobus 11.2 0.4 8.4 0.6 Diplogaster 5.3 0.9 Eucpehalobus 2.3 0.6 3.5 0.4 Leptolaimus 4.0 0.2 Monhystera 2.2 0.0 3.4 0.6 Panagrolaimus 20.1 0.5 35.6 1.7 Plectus 6.2 0.6 1.9 0.4 Pleodera 7.1 0.4 1.7 0.3 Prismatolaimus 5.6 0.7 2.5 0.6 Rhabditis 33.6 1.4 4.4 0.4 Wilsonema 2.2 0.8 2.3 0.6 Fungus Feeding Aphelenchoides 16.4 1.8 10.0 0.6 Aphelenchus 16.6 0.9 4.8 0.5 Diphterophora 5.2 0.2 3.0 0.4 Ditylenchus 5.1 0.2 Tylencholaimus 4.1 0.3 2.2 0.4 Predatory Actinolaimus 1.5 0.1 Aporcelaimus 2.1 0.4 Monochromadora 13.3 0.2 2.1 0.2 Mononchus 3.5 0.3 1.7 0.2 Seinura 4.0 0.3 2.2 0.2 Omnivores Actinolaimus 2.1 0.1 Belondira 1.0 0.3 Campydora 12.9 0.5 1.9 0.3 Discolaimus 5.1 0.4 Dorylaimus 9.3 0.5 1.8 0.2 Eudorylaimus 4.2 0.3 1.6 0.2 Leptolaimus 1.2 0.4 Mesodorylaimus 6.1 0.2 1.4 0.2

118 Continued

Table 4.1 continued

Tripyla 8.2 1.4 Plant Parasitic Aglenchus 3.0 0.2 1.0 0.0 Filenchus 16.5 1.2 25.6 1.3 Helocitylenchus 5.2 2.6 11.4 1.1 Hemicriconemoides 4.2 1.2 Hemicyclophora 1.3 1.5 Heterodera 6.5 1.2 1.0 0.0 Longidorus 5.2 0.9 Paratylenchus 18.5 1.2 5.6 0.6 Pratylenchus 4.2 0.2 Psilenchus 2.5 0.1 Rotylenchus 10.5 1.5 Tylencholaimis 4.2 0.5 1.9 0.3 Tylenchus 3.5 0.5 7.9 0.9 Xiphinema 4.3 0.9 Total number of nematodes 626.0 10.5 346.6 15.5 Number of genera 30.2 0.7 14.2 0.3 Enrichment Index (EI) 76.7 0.5 81.2 0.7 Structure Index (SI) 78.7 0.5 31.7 2.1 Channel Index (CI) 11.9 0.8 6.0 0.6 Maturity Index (MI) 2.2 0.0 1.7 0.0 Plant-Parasitic Index (PPI ) 2.3 0.1 2.2 0.0 Combined Maturity Index (CMI ) 2.3 0.0 1.9 0.0

119

Figure 4.2: Mean (± S.E.) total abundance and abundance of bacteria feeding, fungus feeding, plant parasitic, omnivorous and predatory nematodes (extracted from 10g soil) in turf-grass plots with transplanted forest soil core and plots with commercially available, greenhouse heated topsoil spread on the surface, across a time period of 8 weeks. Letters over bars indicate significant difference significant differences in the treatments in individual week at P ≤ 0.05. 120 nematode genus (Table 4.1). The nematode community in the GrossJean woodlots consisted of around 45% BF, 18% PP, 13% FF, 8% PR and approximately 14% OM nematodes. Also there were significant differences between the SI, CI, MI, PPI and CMI between the two habitats (Table 4.1). After the establishment of treatments in turfgrass plots, the total abundance of nematodes varied from week 1 to week 8, decreasing over time (F = 40.2; df = 5,

20; P < 0.001), with abundance in week 1 being significantly higher than weeks 6 and 8 (Figure 4.2). There was no significant difference between the two treatments across time and there was also no significant interaction between time, treatment and distance. Abundance of BF nematodes declined over time and was significantly lower in weeks 6 and 8 compared to week 1 (F = 16.61; df = 5, 20; P

< 0.001). There were no differences in BF nematode abundance between the two treatments in any of the weeks, except week 6 (F = 17.21; df = 1, 29; P < 0.001) where the population in the core transplant treatment was lower than the commercial topsoil treatment (Figure 4.2). Also there were significant interactions between time and treatment (F = 2.61; df = 5, 20; P = 0.05); and time, treatment and distance (F = 2.41; df = 10, 40; P = 0.02). There was a significant effect of the sampling distance on BF nematode abundance in week 3 (F = 6.73; df = 2, 29; P < 0.01) with abundance at 30cm being lower than 15 or 45 cm in the core transplant treatments (Figure 4.3). Abundance of fungus feeding nematodes decreased initially and then increased by week 8, with no significant difference in abundance between week 1 and 8 in the core transplanted plots (Figure 4.2).

121

Figure 4.3: Mean (± S.E.) values for abundance of bacteria feeding, fungus feeding, plant parasitic, omnivorous and predatory nematodes in turf-grass plots with transplanted core and plots with commercially available, greenhouse heated topsoil spread on the surface, at 15, 30 and 45cm distances across a time period of 8 weeks. Letters over bars indicate significant difference between the two treatments in that individual week at P ≤ 0.05

122

Figure 4.3 continued

123

However, it continuously decreased in the commercial topsoil treatment. Overall, by week 6 and 8 their abundance in plots with transplanted core was significantly higher than the commercial topsoil (F = 19.45; df = 1, 29; P < 0.001) treatment.

There was also a significant interaction between time and distance in the core transplant and commercial top soil treatments (F = 2.12; df = 10, 40; P < 0.05)

(Figure 4.3). Abundance at 15 and 45 cm was significantly higher than 30 cm in week 1 at P < 0.05. Abundance of PP nematodes also varied with time (F =

11.12; df = 5, 20; P < 0.001) showing an overall decreasing trend over 8 weeks

(Figure 4.2). However there was no effect of treatment or sampling distance over time.

Abundance of predatory nematodes showed a significant effect of time (F

= 4.83; df = 5, 20; P < 0.001) as it increased in the core transplanted plots by week 2 and remained significantly higher than the commercial topsoil treatment till week 8 (Figure 4.2). Their abundance in the core transplanted plots stayed significantly higher than that in commercial topsoil treatment. There was no significant interaction of time and distance except in week 1 (F = 6.76; df = 1, 29;

P < 0.001) where abundance at 15 cm was significantly higher than 30 or 45 cm

(Figure 4.3). Differences in the individual weeks were all significant at P < 0.05.

Similarly, omnivorous nematode population increased over time (F = 4.9; df = 5,

20; P < 0.01) and there was a significant interaction between time and treatment

(F = 8.15; df = 5, 20; P < 0.01) (Figure 4.2). Core transplanted plots had a significantly higher abundance of OM at P < 0.05 after week 2.

124

SI showed a significant effect of time (F = 46.29; df = 5, 20; P < 0.001) and an interaction between time and treatment with plots containing transplanted core having a significantly higher SI than commercial topsoil treatment (F = 8.29; df =

5, 20; P < 0.01) (Figure 4.4). These differences were significant from week 2 till the end of the study at P < 0.05. Channel index showed a significant effect of time (F = 17.98; df = 5, 20; P < 0.001) and the interaction of time and treatment

(F = 2.28; df = 5, 20; P = 0.04) with CI in core transplanted plots being significantly higher than the commercial topsoil plots in weeks 6 and 8 at P <

0.05. Maturity index also showed a significant difference across time (F = 37.94; df = 5, 20; P < 0.001) and a significant interaction between time and treatment (F

= 10.32; df = 5, 20; P < 0.001) with a higher MI in the core transplanted as compared with the commercial topsoil plots from week 2 onwards. There were no significant differences among the treatments in week 1. CMI increased over time in the core transplanted plots showing a significant effect of time (F = 35.69; df = 5, 20; P < 0.001) and interaction between time and treatment (F = 8.25; df =

5, 20; P < 0.001). The core transplanted plots had a CMI significantly higher than the commercial topsoil treatment in weeks 2, 3, 6 and 8 at P < 0.05. Enrichment index in both treatments was higher than 70 throughout the 8 weeks and showed no significant difference among five treatments. Plant parasitic index did not show any significant variation across the time period of 8 weeks and there was no effect of treatment across time. There were no apparent differences in grass or

125

Figure 4.4: Mean (± S.E.) values for enrichment index, structure index, channel index, maturity index, plant parasitic index and combined maturity index in turf-grass plots with transplanted core and plots with commercially available, greenhouse heated topsoil spread on the surface, across a time period of 8 weeks. Letters over bars indicate significant difference between the two treatments in individual weeks at P ≤ 0.05

126 weed growth among the three treatments during the 8 weeks to warrant a formal assessment.

Effectiveness of soil core transplants with or without organic amendments in urban vacant lots:

The baseline nematode community in the vacant lots had BF and PP nematodes making up more than 80% of the total nematode population in both the lots. Lot A had approximately 10% FF, 1% PR and 1% OM nematodes, whereas lot B had around 12% FF, 2% PR and 1% OM nematodes. Panagrolaimus,

Acrobeles and Cephalobus were the more commonly found BF genera in Lot A, while Panagrolaimus, Acrobeloides and Cephalobus were more commonly observed in lot B (Table 4.2). Filenchus, Tylenchus, Helicotylenchus and

Paratylenchus were the common PP nematodes in both the lots. The Waterman woodlots on the other hand had an average of more the 17% OM and around 11%

PR nematodes. Approximately 50% of the population was BF, 10% PP and 10%

FF nematodes. There were significant differences between the total number of nematodes, SI, CI, MI and CMI between the two different habitats (Table 4.2).

Soil chemical analysis: Soil heavy metal concentrations in Lot A ranged from 115 to 125 mg/kg Pb, 196 to 248 mg/kg Zn, 1 to 1.2 mg/kg Cd, 19 to 22 mg/kg Cr and 18 to 21 mg/kg As. The concentrations in Lot B varied from 82 to

126 mg/kg Pb, 193 to 310 mg/kg Zn, 1.2 to 2 mg/kg Cd, 25 to 58 mg/kg Cr and

19 mg/kg As. Heavy metal concentrations in the Waterman woodlot area were as follows: (waiting for the final analysis from STAR Lab, OARDC) Soil pH at both

127

Table 4.2: Mean abundance and standard error of mean (SEM) for total numbers of nematodes and genera, and nematode genera belonging to different trophic groups along with the calculated community indices from soil samples (10 g each) collected from Waterman farm woodlot and the vacant lots in Weinland Park neighborhood in Columbus, Ohio

Weinland Park vacant lots Waterman Woodlot Lot A Lot B Trophic guilds/indices Nematode genus Mean SEM Mean SEM Mean SEM Bacteria Feeding Acrobeles 16.5 0.4 12.0 0.8 Acrobeloides 15.2 0.5 12.4 0.9 Alaimus 4.0 0.1 1.8 0.4 1.3 0.3 Cephalobus 11.2 0.4 8.5 0.9 8.3 0.8 Diplogaster 5.3 0.9 Eucpehalobus 2.3 0.6 3.6 0.5 3.5 0.5 Leptolaimus 4.0 0.2 Monhystera 2.2 0.0 4.0 1.0 3.0 0.7 Panagrolaimus 20.1 0.5 33.7 1.7 37.7 2.9 Plectus 6.2 0.6 2.1 0.6 1.6 0.2 Pleodera 7.1 0.4 1.0 0.0 2.0 0.4 Prismatolaimus 5.6 0.7 2.2 0.5 3.0 1.2 Rhabditis 33.6 1.4 5.0 0.7 3.7 0.4 Wilsonema 2.2 0.8 2.5 0.7 1.0 * Fungus Feeding Aphelenchoides 16.4 1.8 10.9 0.8 9.0 0.9 Aphelenchus 16.6 0.9 4.6 0.6 4.9 0.7 Diphterophora 5.2 0.2 4.0 0.6 1.9 0.4 Ditylenchus 5.1 0.2 Tylencholaimus 4.1 0.3 2.4 0.5 2.0 0.3 Predatory Actinolaimus 1.5 0.1 Aporcelaimus 2.1 0.4 Monochromadora 13.3 0.2 1.7 0.2 1.8 0.3 Mononchus 3.5 0.3 2.5 0.3 1.5 0.2 Seinura 4.0 0.3 2.2 0.3 2.1 0.3 Omnivores Actinolaimus 2.1 0.1 Belondira 1.0 0.3 Campydora 12.9 0.5 1.8 0.4 2.0 0.4 Discolaimus 5.1 0.4 Dorylaimus 9.3 0.5 1.8 0.2 1.8 0.2 Eudorylaimus 4.2 0.3 1.1 0.1 2.0 0.3

Leptolaimus 1.2 0.4 Continued 128

Table 4.2 continued

Mesodorylaimus 6.1 0.2 1.7 0.3 1.0 0.0

Tripyla 8.2 1.4 Plant Parasitic Aglenchus 3.0 0.2 1.0 0.0 Filenchus 16.5 1.2 25.1 2.0 26.1 1.8 Helocitylenchus 5.2 2.6 10.4 1.6 12.4 1.5 Hemicriconemoides 4.2 1.2 Hemicyclophora 1.3 1.5 Heterodera 6.5 1.2 1.0 0.0 Longidorus 5.2 0.9 Paratylenchus 18.5 1.2 4.5 0.8 6.5 0.9 Pratylenchus 4.2 0.2 Psilenchus 2.5 0.1 Rotylenchus 10.5 1.5 Tylencholaimis 4.2 0.5 1.8 0.4 Tylenchus 3.5 0.5 8.6 1.3 7.1 1.3 Xiphinema 4.3 0.9 Total number of nematodes 626.0 10.5 307.3 19.3 387.6 23.1 Number of genera 30.2 0.7 14.7 0.5 13.7 0.4 Enrichment Index (EI) 76.7 0.5 80.8 1.0 81.5 1.1 Structure Index (SI) 78.7 0.5 36.0 3.0 27.1 2.9 Channel Index (CI) 11.9 0.8 9.7 0.9 8.3 0.8 Maturity Index (MI) 2.2 0.0 1.7 0.0 1.6 0.0 Plant-Parasitic Index (PPI) 2.3 0.1 2.2 0.0 2.2 0.0 Combined Maturity Index (CMI) 2.3 0.0 1.9 0.0 1.8 0.0

129 vacant lots and the Waterman farm ranged from 7.4 to 7.5. Antecedent soil moisture in the vacant lots varied from 23 to 28%, while it was 28% in the

Waterman farms.

Nematode community in the organic compost and organic peat: Samples from organic compost and organic peat amendments were analyzed for their native nematode community composition. Only 6 genera (Rhabditus,

Panagrolaimus, Monhystera, Acrobeles, Acrobeloides and Cephalobus) were observed in the organic compost samples, with abundance ranging from 15 to 30 nematodes /10g soil, all of which belonged to BF group. Structure index, CI and

PPI could not be calculated however, EI was 94 and MI was 1.2. In the organic peat samples, a total of 10 genera, namely Rhabditus, Diplogaster,

Panagrolaimus, Acrobeles, Cephalobus and Eucephalobus from the BF group;

Aphlenchus from FF group, Dorylaimus from the OM group and Filenchus and

Paratylenchus from the PP nematode group were observed. Their abundance ranged from 19 to 59 nematodes /10g soil. Bacteria feeding nematodes were the dominant feeding type making up 79% of the population, 11.5% were FF, 4%

OM, and 5% PP nematodes in the peat. There were no PR nematodes in any sample. Enrichment index was close to 59, SI < 17.5, CI close to 15, MI < 1.7 and PPI < 2. There were no nematodes in the grass clippings.

Changes in nematode community structure after forest soil core transplantation: Multivariate repeated measures analysis of variance (MANOVA) using the Wilk’s Lambda test of significance showed a significant change in total

130 abundance of nematodes over time (F = 4.63; df = 1, 48; P = 0.036). Figure

4.5(A) shows that total abundance in week 11 in all treatments and in the control was significantly lower than that in week 1, except for the control treatment that did not receive any core, but had compost top-dressing. Moreover individual weeks also showed significant differences, with the abundance in the core + compost treatment being significantly higher than the other treatments and control in week 2 (F = 2.31; df = 4, 89; P = 0.05), week 3 (F = 3.0; df = 4, 89; P = 0.02), week 4 (F = 3.58; df = 4, 89; P = 0.01) and week 8 (F = 2.49; df = 4, 89; P =

0.05). In weeks 1 and 6, core + compost had the highest abundance, closely followed by the core + grass amendment. Abundance of BF nematodes varied significantly with time (F = 85.19; df = 6, 70; P < 0.001) with a gradual decrease by week 11 (Figure 4.5(B)). There was a significant effect of treatment over time

(F = 2.33; df = 24, 245.41; P < 0.05). There was a significant effect of treatment in week 2 (F = 8.16; df = 4, 89; P < 0.001) with higher BF nematodes in core and core + compost treatments, week 3 (F = 5.31; df = 4, 89; P < 0.001) with higher

BF in core + compost followed by core + grass, week 4 (F = 2.54; df = 4, 89; P =

0.04) and week 8 (F = 4.55; df = 4, 89; P < 0.01) with higher BF in core + compost and in control with only organic compost treatments, week 6 (F = 3.44; df = 4, 89; P = 0.01) with highest BF abundance in core + compost treatment, and week 11 (F = 4.21; df = 4, 89; P < 0.01) with core + peat amendment showing the least amount of BF nematodes.

131

Multivariate analysis showed that abundance of FF nematodes also varied with time (F = 5.19; df = 6, 70; P < 0.01) increasing in the core + compost treatment by week 4 and then decreasing back to the levels observed in week 1

(Figure 4.5(C)). Also, distance had a significant interaction with time (F = 1.79; df = 12, 140; P = 0.05). Univariate analysis, on the other hand, showed significant interaction between time and treatment (F = 1.59; df = 24, 450; P =

0.04), and the results for the individual weeks were as follows. Distance was a significant variable for week 2 (F = 8.59; df = 2, 89; P < 0.001) and week 6 (F =

4.25; df = 2, 89; P < 0.05), while treatment was a significant variable in week 3 (F

= 5.05; df = 4, 89; P < 0.01) with higher FF abundance in the core + compost and core + peat treatments being significantly higher than the others and in week 4 (F

= 8.16; df = 4, 89; P < 0.001) with highest FF in core + compost amendment.

Multivariate analysis also showed that PR nematodes varied significantly with time (F = 72.73; df = 6, 70; P < 0.001), increasing in abundance from week 2 to week 4; with treatment across time (F = 4.77; df = 24, 245; P < 0.001), showing significantly higher abundance in core + compost amendment; and with the distance across time (F = 1.8; df = 12, 140; P = 0.05) (Figure 4.5(D)).

Individual week analysis showed that PR abundance varied with treatment and with distances in weeks 1, 2, 3 and 6 (df = 4, 89 and 2, 89 respectively at P <

0.05). In weeks 1 and 3 the core, core + compost and core + grass treatments had significantly higher PR nematodes, and in weeks 2 and 6 abundance in no core + compost amended plots was the lowest. Also, there abundance at 15 cm distance

132 was significantly higher than the other two distances in weeks 1, 2, 3 and 6.

Weeks 4, 8 and 11 showed a significant interaction with treatment alone (df = 4,

89; P < 0.05) with abundance in core + compost amended plots being the highest and that in core + peat and no core + compost amended plots being significantly lower. Multivariate analysis also gave a significant interaction between treatment and distance of sampling over time in weeks 2 (F = 5.39; df = 8, 89; P < 0.001) and 3(F = 2.21; df = 8, 89; P = 0.03).

Similar to PR nematodes, OM nematodes also showed significant increase in abundance over time (F = 107.17; df = 6, 70; P < 0.001), significant interaction between treatment and time (F = 4.69; df = 24, 245; P < 0.001), and between distance and time (F = 2.61; df = 12, 140; P < 0.01) (Figure 4.5(E)). Significant interactions between time and treatment were observed at all of time points (df =

4, 89; P < 0.01). Highest abundance of OM nematodes was observed in core + compost treatment from week 2 to 6, however, generally core and core + grass amended plots also showed high abundance of OM nematodes. Plots that did not receive any core transplantation had the lowest abundance of OM nematodes consistently throughout the study. Plant parasitic nematode abundance decreased over time (F = 47.57; df = 6, 70; P < 0.01) and also showed an interaction with treatment over time (F = 2.83; df = 24, 245; P < 0.01) using the Wilk’s Lambda multivariate analysis (Figure 4.5(F)). A significant effect of treatment on PP nematode abundance was seen individually in weeks 1 (F = 3.23; df = 4, 89; P =

0.01), 3 (F = 2.59; df = 4, 89; P = 0.04), 4 (F = 4.53; df = 4, 89; P < 0.01) and 6

133

Figure 4.5:Means +SEM (standard error of mean) of total nematode abundance and abundance of different feeding types: bacteria feeding, fungus feeding, plant parasitic, omnivorous and predatory nematodes (per 10g soil), in the two vacant lots in Weinland Park, Columbus, Ohio, over a time period of 11 weeks after forest soil core transplantation, under different organic amendments. Letters on top of the bars indicate significant differences between the treatments within each week.

134

(F = 5.44; df = 4, 89; P < 0.01). Overall, the PP nematodes abundance decreased in all core containing treatments over the 11 week time period, however, in the plots that did not receive the core transplantation, the abundance in week 11 was not statistically different from that in week 1.

Enrichment index remained greater than 70 for all treatments for the time period of the study however there were some differences in the individual weeks

(Figure 4.6(A)). There was a significant effect of time on EI (F = 7.93; df = 6, 70;

P < 0.01), along with an effect of treatment over time (F = 3.97; df = 24, 245; P <

0.01). Differences were observed in week 2 (F = 8.36; df = 4, 89; P < 0.01) , week 3 (F = 2.41; df = 4, 89; P = 0.05), week 4 (F = 7.19; df = 4, 89; P < 0.01), week 6 (F = 3.48; df = 4, 89; P = 0.01), week 8 (F = 6.69; df = 4, 89; P < 0.01) and week 11 (F = 4.43; df = 4, 89; P < 0.01). Towards the end in weeks 8 and 11 the plots with only core showed a greater EI than any of the other treatments.

Multivariate repeated measures analysis for SI showed a significant effect of time on SI (F = 210.31; df = 6, 70; P < 0.01), treatment over time (F = 2.61; df = 24,

245; P < 0.01), and a significant interaction between time and distance of sampling from the core edge (F = 1.57; df = 12, 140; P = 0.01) (Figure 4.6(B)).

SI was significantly higher in all the core containing plots when compared to the plot that did not receive the core transplantation (df = 4, 89; P < 0.01). Also, among the core containing plots it was significantly higher in the plots with core, core + compost and core + grass, as compared to core + peat amended plots (df =

4, 89; P < 0.05). Results for MI were very similar to SI with significant increase

135 in MI observed across time (F = 293.05; df = 6, 70; P < 0.001), along with significant interactions between time and treatment (F = 7.97; df = 24, 245; P <

0.01) where MI for all core containing treatments was higher than the MI for plots that did not receive the core. The interaction between time and distance (F =

1.57; df = 12, 140; P < 0.001) was significant (Figure 4.6(C)). Plant parasitic index showed only minor variations over time (Figure 4.6 (D), with a significant

Wilk’s Lambda statistic for time (F = 19.60; df = 6, 70; P < 0.001) and interaction between time and treatment (F = 1.86; df = 24, 245; P = 0.01). These significant effect were observed in week 1 (F = 3.12; df = 4, 89; P = 0.02) where PPI in core

+grass amended plots was significantly higher than the other treatments; and in week 11 (F = 4.58; df = 4, 89; P < 0.01), where both the core and core + compost plots had significantly higher PPI than the core + grass and no core + compost amended plots.

Higher trophic level OM and PR nematode abundance data from all the plots that received core transplantation was subjected to Wilk’s Lambda multivariate repeated measures analysis to check for overall interaction between distance of sampling and time with all treatments considered together. Significant differences were found for OM (F = 2.43; df = 12, 110; P < 0.01) but not for PR nematodes. Additionally, in the core containing plots that did not receive any organic amendment, OM nematodes abundance significantly increased at 15 cm in weeks 2 and 3 as compared to 30 and 45cm distances. Towards the end in week 8 and 11, there were no significant differences between the 3 distances

136

Figure 4.6: Means +SEM (standard error of mean) of calculated nematode community indices including enrichment index, structure index, maturity index and plant parasitic index, in the vacant lots in Weinland Park, Columbus, Ohio, over a time period of 11 weeks after forest soil core transplantation under different organic amendments. Letters on top of the bars indicate significant differences between the 3 organic amendments within each week.

137

(Figure 4.7). For the other organic amendments, abundance at 15 and 30 cm increased at the same rate. Predatory nematode abundance also followed a similar pattern of increasing at 15 and 30 cm distances by week 3, with no significant differences among the distances by week 8 (Figure 4.8). Abundance of both higher trophic level nematode groups was significantly higher in week 11 as compared to week 1in all core transplanted plots.

Overall, by week 11, the composition of the nematode community had changed significantly (Table 4.3). In the plots that received core transplantation, the abundance of

BF decreased to 28 to 37% of the total nematode community while in the control without any core, it was 42%. Abundance of PP nematodes varied from 26 to 32% among the different treatments with the highest abundance in core + peat treatment. FF abundance also varied from 13 to 20%, with a higher proportion in core + peat and core + compost treatments. Abundance of PR and OM nematodes had increased significantly by week

11in the core containing plots ranging from a low of 4 and 8% respectively in the core + peat plots to a high of 12.6% PR nematodes in the grass amended plots and a high of

14.5% OM nematodes in only core containing plots. The control plots that did not receive any cores had only 3% OM and PR nematodes. Also the abundance of c-p scale

4 nematodes increased to 11 to 20% of the total population. The ratio of BF to totalpportunists showed a decrease in value in all core transplanted plots indicating a shift in the energy transfer pathway towards a fungal dominated system. EI was still maintained at >71 for all treatments, SI showed a large increase in the core containing treatments to >71, while that in the control without any core it was still 48. MI and

138

Figure 4.7: Mean +SEM (standard error of mean) of spread and abundance of higher trophic level omnivorous nematodes at 15, 30 and 45cm distances around the transplanted forest soil core, in the vacant lots in Weinland Park neighborhood in Columbus, Ohio, under different organic amendments. Graphs (A) represents only core with no organic amendment, (B): core + compost, (C): core + grass and (D): core + peat amendment. Letters on bars indicate significant differences between the distances in each week.

139

Figure 4.8: Mean +SEM (standard error of mean) of spread and abundance of higher trophic level predatory nematodes at 15, 30 and 45cm distances around the transplanted forest soil core, in the vacant lots in Weinland Park neighborhood in Columbus, Ohio, under different organic amendments. Graphs (A) represents only core with no organic amendment, (B): core + compost, (C): core + grass and (D): core + peat amendment. Letters on bars indicate significant differences between the distances in each week.

140

Table 4.3: Mean and standard error of mean (SEM) of percent abundance of nematodes classified according to (i) different feeding types, PPN: plant parasitic, BF: Bacteria feeding, FF: Fungus feeding, PR: Predatory and OM: Omnivorous nematodes; (ii) colonizer-persister (C-p) scale, (iii) the ratio of bacterivores to total opportunistic nematodes and (iv) calculated nematode community indices, EI: enrichment index, SI: structure index, CI: channel index, MI: maturity index, PPI: plant parasitic index, and CMI: combined maturity index; for Oct 2013 (week 11 of the study) in vacant lots in Weinland Park neighborhood in Columbus, Ohio, under different treatments.

Only core Core + compost Core + grass Core + peat Only compost Mean SEM Mean SEM Mean SEM Mean SEM Mean SEM PPN 27.4 2.6 28.1 3.3 26.3 2.3 32.2 3.2 32.0 4.2 BF 37.2 2.1 32.5 2.7 31.9 2.0 27.9 2.8 42.3 3.4 FF 13.4 0.9 19.3 1.6 14.3 1.8 17.6 1.3 11.5 1.1 PR 7.5 0.9 9.9 0.6 12.6 0.8 4.3 0.7 3.1 0.8 OM 14.5 1.2 13.1 1.0 11.9 1.3 8.1 0.8 3.1 0.6 C-p 1 25.3 1.7 17.9 1.7 16.3 2.2 14.3 1.7 23.4 2.3 C-p 2 34.4 1.9 35.0 2.5 44.9 2.0 46.8 2.4 57.2 2.8 141 C-p 3 19.7 2.7 31.0 3.4 23.1 1.9 27.8 3.5 14.5 2.3 C-p 4 20.5 1.7 15.7 1.2 15.6 1.4 11.0 1.0 4.7 0.7 C-p 5 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 BF/(BF+FF) 0.7 0.0 0.7 0.0 0.6 0.0 0.6 0.0 0.9 0.0 EI 83.1 1.2 77.6 1.5 72.1 3.3 71.9 1.8 76.5 2.6 SI 80.0 1.5 81.0 1.3 78.5 1.7 71.6 2.9 48.2 2.3 CI 10.5 0.9 12.5 2.0 21.6 5.4 21.3 1.5 12.2 2.9 MI 2.3 0.0 2.4 0.0 2.4 0.0 2.3 0.0 1.9 0.0 PPI 2.5 0.1 2.5 0.1 2.3 0.0 2.3 0.0 2.4 0.1 CMI 2.4 0.0 2.5 0.0 2.1 0.0 2.4 0.0 2.0 0.0

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Figure 4.9: Temporal dynamics of the nematode food web in vacant lots in the Weinland Park neighborhood in Columbus, Ohio, from August 2013 to October 2013, before and after transplantation with an intact forest soil core, with different organic soil amendments applied in August 2013.

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CMI values in al treatments also increased to > 2.3.

Nematode faunal profile analysis (Figure 4.9) showed that the core transplantation with or without the addition of organic amendments improved thestructural complexity of the soil food web within 11 weeks pushing the food webs to Quadrant B. Plots with only core transplantations saw an improvement in

SI by approximately 60%, core + compost improved by 62%, core + grass by

57%, core + peat amendment by 43% as compared to the SI before core transplantation, whereas SI in plots that did not receive the core but were amended with compost decreased by 3%.

Discussion

The results of this study support the hypothesis that the missing nematode higher trophic guilds (along with their associated organisms) can be successfully transferred from an ecosystem with a mature and well-structured food web via small intact soil cores (636 cm3) into a new ecosystem lacking those guilds. The results showed that nematodes rapidly moved out of the transplanted forest soil cores and colonized the surrounding area both in turfgrass plots and urban vacant lots. The opportunistic BF nematodes moved out of the transplanted forest cores into autoclaved soil in microcosms first, utilizing the available soil carbon and nutrients, and establishing large populations within 2 weeks. The higher trophic level OM and PR nematodes followed and could be detected in the soil

143 surrounding the core by week 3. This initial experiment confirmed the potential of a small “intact” soil core from an ecosystem with a mature and structured soil food web to serve as an inoculum for restoration of the soil food web in a nutrient rich but enemy-free environment within two to three weeks. Alteration of the soil food web composition by other means such as modification of above ground plant diversity, may take several months to years for the soil food web to return to its natural complexity via natural succession (Palmer et al., 1997), depending upon the site history and opportunities for re-colonization from the surrounding areas.

Leguminous cover crop rotations can help modify the microbial composition of soil (Stirling et al., 2002) by altering the bacterial and fungal abundance in plant root rhizosphere, however they are time consuming, requiring one or more growing season(s) and the cover crops may be specific to a geographic region.

Moreover, they do not specifically introduce beneficial, higher trophic invertebrate guilds into the food web. While there were no significant differences in the abundance of BF and FF nematodes across different distances from the soil core, OM and PR nematodes were more abundant closer to the core edge than at a distance of 20 cm. This may be due to their slow mobility, large body size, long generation time and low rates of reproduction (Ferris et al., 2001).

In addition to transferring a mature nematode community, the forest soil core may also transfer other soil micro-fauna including beneficial bacteria, fungal spores and hyphae which multiply rapidly in the nutrient rich disturbed soil and function as a food resource for nematodes and other biota, further promoting

144 nutrient cycling (Pavao-Zuckerman and Coleman, 2007) and adding multiplicity of energy transfer channels in the food web. Other bacterial inoculation techniques commonly used in agriculture include seed, root and tuber coatings, and plant tissue inoculum in synthetic or peat/clay based carrier molecules

(Kloepper et al., 1989; Elsas and Heijen, 1990). Survival of such laboratory cultured bacterial inoculants however, depends on several environmental parameters such as soil texture, pH, moisture, competition from native soil bacteria and their ability to survive sudden exposure to harsh environmental conditions once the carrier molecule breaks down (Elsas and Heijen, 1990).

Developing carrier materials such as synthetic adhesives to coat around seeds

(Elegba and Rennie, 1984), customization to optimum survival conditions of specific bacterial strains, culturing and storage of tissue inoculum (Elsas and

Heijen, 1990) also require additional resources. On the other hand, transplantation of an intact soil core avoids these externalities and is not limited to transferring a single beneficial bacteria or fungal species. About 636 cm3 soil

(volume of soil in one core) may contain thousands of different bacteria, protozoa, detritus based microbes, fungal hyphae, mites, collembolans, and beneficial arthropods such as spiders and other predatory species. The core can be collected from undisturbed wooded areas close to the recipient ecosystem to ensure maximum compatibility of soil properties, while adjustments to pH, moisture, bulk density, and nutrients can be made to ensure survival of the introduced biota.

145

Soil cores for transplanting into the turfgrass lots and in the urban vacant lots were collected from nearby (less than 6 km) forest ecosystems. Soils in these forest ecosystems had mature food webs with much greater proportions of higher trophic level OM and PR nematodes than found in the contiguous urban or agricultural landscapes. The high MI and SI values indicated an uninterrupted ecological successional pathway that had allowed the more sensitive nematodes from higher trophic guilds to flourish in the soil community, hence indicating a less disturbed environment (Ferris and Bonger, 2006; Neher, 2001; Ferris et al.,

2001; Yeates et al., 1993). Both forests had SI > 76 and MI > 2.2 representing a rich vertical trophic complexity of nematodes.

Transplantation of forest soil cores in turfgrass plots included interactions between the introduced nematodes and the associated biotic and abiotic factors with the resident communities potentially affecting the establishment of the introduced species. Soil temperature is a critical variable that determines microbial activity (Zak et al., 1999) and declining soil temperature from August through October may have been one of the reasons for an overall decreasing trend in nematode abundance in both the commercial topsoil and core transplant treatments. Abundance of FF nematodes in the core transplanted plots did not increase over time however it was significantly higher than the commercial topsoil treatment in week 8. This shows that fungal growth in the core treatment plots achieved a steady growth rate and was able to sustain a stable population of the FF nematodes over time, as opposed to the commercial topsoil treatment

146 where the population of FF decreased gradually. Abundance of PP nematodes was not significantly different among the two treatments, indicating that the transplanted cores did not introduce any harmful PP genera into the community.

A greater abundance of OM and PR nematodes in the core containing plots along with a higher SI and MI throughout the sampling duration showed successful establishment of higher tropic diversity in the turfgrass ecosystem. This would allow the disturbed soil ecosystem to regain beneficial ecological services including nutrient and energy flows and biological control of pest species (Pavao-

Zuckerman and Coleman, 2007). Commercial topsoil did not improve the complexity of the soil food web over the 8-week period and hence we conclude that the standard procedures followed for excavating, transporting and storing large quantities of commercial topsoil are not ecologically sound. Such practices result in depleting the soil food web of sensitive microbial and invertebrate species. Instead, the same ecosystem that is used as a source of commercial topsoil could be used more efficiently for removing smaller, intact soil cores that can successfully replenish the food web structure in the recipient ecosystem, while preserving the ecological integrity of the exporting ecosystem.

The turfgrass plots in our study had high EI and a high abundance of r- selected colonizing BF, FF, and PP nematode guilds that could have served as a food resource for the introduced predatory and omnivore nematodes, enabling their establishment without significant predation or competition (Hedlund et al.,

2004). Also due to the already established nematodes belonging to c-p scales 1, 2

147 and 3, changes in the abundance of BF, FF or PP nematodes were not significant across different distances from the edge of the transplanted core.

Baseline data from the urban vacant lots also showed a high EI with abundance of BF and PP nematodes. It is expected as urban vacant lots undergo extensive soil disturbance such as compaction due to heavy foot traffic or machinery, soil excavation and digging resulting in topsoil displacement, uprooting of preexisting vegetation (USDA, 2009) and possible burial of demolition debris into the lots (Sharma et al., 2014; Cheng and Grewal, 2009). It has been predicted that re-establishing the lost microbial populations in such disturbed ecosystems through natural processes could take upwards of several decades through natural succession (Belnap, 1995), or through conventional methods such as modifying plant communities or use of cover crops. The lots in

Weinland Park neighborhood used in this study had been vacant for more than 8 years and still had a SI lower than 40. This could be due to the lack of opportunities for re-colonization for less mobile soil fauna, especially in fragmented urban landscapes (Bryant, 2006; Mckinney, 2002; Wang and

Moskovite, 2002; Byrne and Grewal, 2009), which was the case in our study sites.

Hence, it can be concluded that in an urban scenario or for soil that has undergone intensive disturbance similar to these vacant lots, perhaps even 8 years is not sufficient time for missing higher trophic levels to return to the soil ecosystem in any significant proportions.

148

Additionally, soil in urban vacant lots is often contaminated with heavy metals from past land use, or paint dust originating from the old houses and building that were present on the land (Sharma et al., 2014; McClintock, 2012).

However, our previous studies (Sharma et al., 2014) of the heavy metal concentrations in the vacant lots in the same Weinland Park neighborhood showed that concentrations of As, Cd, Cr and Pb were within the normal background range of these metals in the Franklin county (USGS 2012) and in the state of Ohio (Cox and Colvin, 1996). Only Zn concentration in at least one of the soil samples from both the vacant lots was above the natural background range of 7.5 to 190 mg/kg soil, however the concentration was much lower than the USEPA established Soil Screening level (SSL) for direct soil ingestion by humans (23,000 mg/kg soil). Hence, these vacant lots may be used as a garden for growing fruits and vegetables, without fear of contaminants being absorbed into the food chain. Similarly, other vacant lots where the metal concentrations are not higher than the SSLs for soil ingestion can be repurposed for urban agriculture.

Conventional organic amendments utilized in urban gardening include compost, manure, biosolids, and municipal solid wastes (Park et al., 2011). We studied the improvement in the soil food web structure in vacant lots via core transplantation in conjunction with compost, grass clippings and peat amendments. Our analysis of the organic compost and peat amendments did not reveal a well-structured nematode community in them. The overall abundance of

149 nematodes was approximately 10 times lower than the forest soil and with a much lower diversity. Both compost and peat did not have any PR nematodes and peat had only a few OM nematodes. Both amendments had nematode food webs with poor SI and MI values. This shows that organic amendments themselves do not supply the soil with any additional beneficial nematodes to help replenish the food web structural complexity. In fact, Cheng and Grewal (2009) showed that in turfgrass plots established on subsoil amended with organic compost did not have any higher trophic level nematodes even after two years. This was also corroborated by the absence of any change in the enrichment and structural indices of the soil food webs in plots amended with only compost in the current study. Thus, management of urban gardens solely with organic amendments is not sufficient for reconstruction of the structural complexity of the soil food web to its natural state.

Analysis of the individual feeding types in the nematode community showed that abundance of BF nematodes was initially higher in the compost amended plots. This could be due to the availability of a labile source of carbon which may have resulted in their exponential growth (Nicolardot et al., 2001;

Parnas, 1875). However, towards the end of 11 weeks, BF nematode abundance was similar in all treatments except for core + peat amendment, which had a lower abundance. Different nematode feeding types dominate the soil food web depending on the composition of organic amendment used (Ferris and Matute,

2003). The high C:N ratio of peat was not a suitable source of food for bacterial

150 growth and hence the low growth of BF nematodes. In contrast, peat may have favored the growth of fungi and FF nematodes (Ferris and Matute, 2003), which was also observed in the higher abundance of FF nematodes (comparable to core

+ compost treatment) in the peat amended plots during the first few weeks (Figure

5). However, towards the end, the abundance of FF nematodes was similar in the core alone plots as well. Abundance of PR and OM nematodes was significantly higher in all the core transplanted plots as compared to the plots that did not receive any core, also translating into higher SI and MI, showing that the intact core can serve as an effective inoculum of the higher level trophic guilds for the urban soil. Structure index in the control without any core remained below 50.

Among all the core transplanted plots, core + organic compost as soil amendment showed the maximum increase in the abundance of OM and PR nematodes; closely followed by the core + grass and only core treatments, respectively.

Abundance of OM and PR nematodes measured at the different distances from the edge of the transplanted core showed that the nematodes moved out and multiplied, reaching the greatest distance of 45 cm within 4 weeks. After 4 weeks the numbers were consistently high till the end of the study. This shows that use of an intact core is a fast and efficient method of reintroducing the missing links to the soil food web, much faster than using cover crops which may take up to a few growing seasons to change the soil microbial community composition

(Stirling et al., 2002).

151

Abundance of PP nematodes did not vary significantly between the treatments and the controls except for weeks 1 and 6 where their abundance was higher in the treated plots. By week 8 and 11 there was no differences in the core and subplots that did not receive any core indicating that transplanting a small intact core did not introduce a large number of PP nematodes. The same however cannot be said for procedures such as topsoil replacement where a truckload of soil that is brought in from an unknown source may bring unwanted pests, parasites or a weed seed bank of invasive species.

Hence, this study has established that core transplantation in urban vacant lots was effective and beneficial to the soil ecosystem by significantly increasing the diversity and complexity of the soil nematode community, and in conjunction, the overall soil ecology. This method of restoring the missing species in the soil community was effective due to the nutrient rich status of soil with an established community of the r-selected species (Chapter 3; Hedlund et al., 2004). Hence, the introduced higher trophic guilds used the available niches in the soil ecosystem that were optimum for these k-selected species, without disrupting the existing soil communities (Cade, 1988). Overall, the results showed that organic compost with a low C:N ratio as soil amendment worked the best in combination with the core transplants to increase MI and SI of the recipient vacant lot soil. This was closely followed by grass and finally peat as soil amendments. This may be partly due to the rapid availability of labile C and N sources from organic compost as opposed to peat which would be more difficult to break down and

152 decompose (Nicolardot et al., 2001; Parnas, 1875). The nutrients are utilized by the existing microbial communities, subsequently providing optimum food resources for the introduced nematode species. Additionally, compost amendments to soil reportedly increase abundance of predatory arthropods as opposed to herbivores, provide better control of weeds and other pests, improve soil structure and aggregate stability, balance out soil pH modified by the presence of paint and construction residues and immobilize heavy metals by associations with humic acids (Perez-Piqueres et al., 2006; Cogger, 2005; Brown and Tworkoski, 2004; Giusquiani et al., 1995) to a greater extent than the other amendments.

In conclusion, effective management of urban agriculture for both sustainable food production and environmental improvement requires an understanding of the soil biological processes (Scherr and McNeely, 2008). As the importance of soil health (Monkiedje et al., 2006; Kibblewhite et al., 2008) has been recognized, the use of compost for sustainable soil management is often recommended (Brown and Tworkoski, 2004). However we show that compost amendments by themselves are not able to replenish the soil food webs with the missing higher trophic links in disturbed urban soils as highlighted previously by

Cheng and Grewal (2009). Our method of bringing in intact soil cores from a forest ecosystem and transplanting them into vacant lots was successful in restoring the functional diversity of the urban soil food web. It not only focused on transferring the missing trophic guilds, but also likely transplanted other

153 associated microbes and arthropods of the native ecosystem, thus enriching soil’s faunal diversity and returning it to its original pre-disturbance state over time.

Also, based on this study, we established that a single intact soil core from a forest area was capable of restoring the food web complexity in a 2.3 m2 area in approximately 4 weeks, with an additional 2-3 weeks required for the population of the higher trophic levels to stabilize in the absence of any physical disturbance to soil. Based on this we can estimate the need for transplantation of a single core

(9 cm dia) every 1.5 m or 1 core for every 2.3 m2 in an urban garden to reconstruct the soil food complexity. It is important to note that the adoption of management strategies such as reduced tillage, optimal soil moisture, and reduction in the use of chemical inputs, would be necessary to help stabilize and maintain the introduced trophic guilds. Future research testing the use of varied core sizes, making use of smaller cores transplanted closer together in urban gardens, or larger cores a farther distance apart in agricultural fields, along with studies in different environmental conditions such as a greenhouse or hoop-house as opposed to an open field, could further refine this technique.

Acknowledgements:

We would like to thank Amr Badway, Dr. Ruisheng An, Dr. Zhiqiang Cheng and

Dr. Harit Bal for all their help in the field work and data analysis.

154

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Chapter 5: Overall Discussion and Conclusions

The overall goal of my thesis was to assess soil quality and health in vacant lots in low income group residential neighborhoods, and to supplement the below-ground soil food web with missing elements that would eventually boost sustainable food production. Hence, enabling local residents to benefit from all potential ecosystem services derived from the empty patches of land. Through my research, I established that all vacant lots in post-industrial communities are not uniformly contaminated and do not require complete topsoil replacement. They can be utilized for community gardens for growing fruits and vegetables.

Additionally, our novel approach of performing intact core transplantations to restore the functional complexity of below-ground soil food web showed encouraging results. I was able to introduce and support the survival of sensitive higher trophic level omnivorous and predatory nematode genera into the vacant lot soil food web via core transplantation, along with the use of organic amendments.

The primary requirement for safe and sustainable urban agriculture is uncontaminated healthy soil. However, soil quality in cities is severely impacted by anthropogenic activities (Kabata-Pendias, 2000; Oldeman, 1994). Intensive

161 industrialization accompanied by excessive soil disturbance, compaction, large scale soil erosion, loss of nutrients and contamination with heavy metals are some of the common characteristics of a degraded urban environment (Karlen et al.,

1997). On the other hand, urban agriculture has seen a steady rise in several cities across the US with almost 15% of the total produce originating within cities

(Duchemin et al., 2008). People who would benefit the most from a local source of fresh fruits and vegetables are the low income residents in an economically disadvantaged neighborhood. Therefore, through my dissertation research I have attempted to assess soil quality in vacant lots in two such neighborhoods, Hough in Cleveland and Weinland Park in Columbus, Ohio.

We found that only 1 lot in the Weinland Park neighborhood and 3 in

Hough had As concentration higher their respective natural background levels in the Franklin and Cuyahoga counties. Only 1 lot in Weinland Park and 15 in

Hough had Pb concentration exceeding the Eco SSL of 400 mg/kg soil/ of 0a few of the vacant lots had As and Pb as a cause of concern with concentrations higher than the USEPA established generic soil screening levels (SSLs) (USEPA 1996).

An important factor determining the concentration of metals in soil is the mineralogical profile and parent bedrock geochemistry (Yesilonis et al., 2008;

Adriano 2001; Kabata-Pendias 2000). Based on the data presented by Venteris et al., (2014), both of the studied neighborhoods are located in areas with high As concentration in the parent bedrock (greater than 20 mg/kg soil), thus a high value of soil As is expected in these areas. This should also be kept in mind when

162 comparisons are drawn with the USEPA SSLs for remediation efforts. The SSL for As set at 0.4 mg/kg soil by the USEPA, is an overly conservative estimate. A large part of central, western and eastern Ohio has background soil As concentrations higher than 10 mg/kg soil, even in areas with minimum anthropogenic influence (Venteris et al. 2014). Based on this there have been suggestions to reassess the remediation guidelines set by USEPA (Venteris et al.,

2014). On the other hand, all of the studied vacant lots in the two neighborhoods had Pb concentrations higher than the average background concentrations in

Franklin and Cuyahoga counties (USGS 2012). Lead is a residual contaminant from use of leaded paint and gasoline (McClintock 2012; Mielke 1994) and the industrial past of the two cities (Warf and Holly 1997; Jennings 2008) and is therefore a more widely acknowledged urban soil contaminant (McClintock 2012;

Mielke 1994). However, based on the generic SSL of 400 mg Pb/kg soil, only 6% of the vacant lots in Weinland Park and 53% in Hough neighborhood had at-least one soil sample with Pb levels higher than the SSL.

This shows that a majority of the vacant lots in both Hough and Weinland

Park neighborhoods could be repurposed as individual or community gardens and used for growing food crops. However, the remaining lots could also be reclaimed based on further tests. Future analysis with soil sampling performed at a greater spatial resolution could help determine patches within the lots with high total metal concentrations. These patches could either be treated by applying phosphate fertilizers, organic matter and compost amendments to stabilize Pb concentrations

163 in soil and decrease its bioavailability (Brown et al., 2003; Basta et al., 2001) or they could be completely avoided. Additionally, increasing soil pH would also make the metals less bioavailable (Brown et al., 2003).

Out of all the vacant lots studied, approximately 94% in Weinland Park neighborhood and 47% in Hough neighborhood may not pose a human health risk with respect to the 5 major metals that were studied (when compared to the natural background concentrations in Franklin and Cuyahoga counties and the

USEPA Eco SSLs), and hence could be used for community gardening.

Establishing community vegetable gardens on these lots would benefit the residents tremendously by supplementing their dietary intake with fresh, healthy food and promoting their social and economic well-being (De Bon et al., 2008;

Duchemin et al., 2008). High production efficiency of the food crop biomass over consecutive growing seasons can be ensured by incorporating maximum biodiversity and multi-trophic interactions in the above and below ground food webs in the urban ecosystem (Duffy et al., 2007). Greater biodiversity would also contribute towards resilience in the urban food gardens against environmental disturbances such as drought or extreme temperatures (Hedlund et al., 2004;

Brussard et al., 2007).

An analysis of the below ground soil food webs in vacant lots (using the soil nematode community as a bio-indicator), revealed that the urban soil food web is severely depleted of the more sensitive, higher trophic level omnivorous and predatory nematodes. Consequently, the food web may be depleted of other

164 higher trophic level micro- and macro-fauna as well (Faeth et al., 2011; Pavao-

Zuckerman and Coleman 2007; Mckinney, 2002). Previous studies have described modified biological compositions in the urban environment with a decrease in the vertical trophic diversity (species diversity across multiple trophic levels) in food chains due to regular anthropogenic disturbances (Faeth et al.,

2011; Goddard et al., 2010; Yeates and Bongers 1999). Furthermore, there is a dearth of published literature about the effect of disturbances and soil heavy metal concentrations on below ground nematode community structure in urban vacant lots, especially in economically disadvantaged residential neighborhoods.

To fill this gap in knowledge I estimated the risk of soil heavy metal concentrations to the soil food web through comparison with USEPA’s Eco SSLs for heavy metal exposure to soil invertebrates. Only Zn concentrations in all the vacant lots exceeded the Eco SSL value of 120 mg/kg soil. I also studied the interaction between soil properties, heavy metal concentrations and the functional diversity of the nematode community in vacant lots in both Hough and Weinland

Park neighborhoods. Results showed that CI was negatively associated with Cd and Zn concentrations concentrations in Weinland Park neighborhood; whereas, soil As, Cd, Cr, organic matter and texture were the significant variables whose interactions influenced the nematode community in the Hough neighborhood.

Both neighborhoods had distinct soil physical and chemical properties and soil contaminant levels based on their previous land use and industrial histories; however these abiotic factors and their interactions significantly influenced the

165 opportunistic lower trophic level nematode abundance in both neighborhoods.

Bacteria and fungus feeding nematodes showed a negative correlation with As concentrations. Channel index, calculated using abundance of fungus and bacteria feeding nematodes also gave a negative correlation with Cd and Zn concentrations in the Weinland Park neighborhood. These correlations hint at the biological importance of the opportunistic lower trophic level nematodes as environmental bio-indicators (Yeates and Bongers 1999) and as indicators of heavy metal stress, in the absence of the sensitive higher trophic guilds.

Anthropogenic disturbances can severely impact soil food web structure.

Events such as demolition of an old building, compaction due to heavy machinery, soil excavation resulting in topsoil displacement, uprooting of preexisting vegetation (USDA, 2009) and burial of demolition debris into the lots can result in elimination of the sensitive species, preventing their return. This can alter the functioning of a soil ecosystem and its derived services such as increased plant biomass and biological control of pests (Scherr and McNeely, 2008; Duffy et al., 2007). Nematode community analysis in two lots in the Weinland Park neighborhood showed that there had been no significant changes in the structural complexity or maturity of the nematode community composition over the last 3 years, when the disturbance event had occurred more than 8 years ago. The community consisted of bacteria feeding and plant parasitic nematodes that made up 80% of the population. Higher trophic level omnivorous and predatory nematodes and those belonging to c-p scales 4 and 5 were found in the lowest

166 proportions. Borer et al. (2006) described how the lack of predatory species from the food web in an ecosystem can significantly impact abundance of species at other trophic levels as well as decrease plant biomass and productivity.

Conventional methods of managing a community garden such as use of organic amendments (compost and biosolids) (Cogger, 2005; Bulluck et al., 2002), fertilizer applications (Sarathchandra et al., 2001; Sterret et al., 1996) and leguminous cover crop rotations (Stirling et al., 2005; Dabney et al., 2001), may enrich soil nutrient levels but not its biological diversity (Cheng and Grewal,

2009). Use of cover crop may be limited spatially and geographically and may require several growing seasons to alter the soil microbial composition.

On the other hand, reconstruction of the vertical functional diversity of the soil food web, using intact cores from forest soil resulted in a significant increase in abundance of omnivorous and predatory nematodes in laboratory microcosms as well as in the field. The forest soil had high structure index values greater than

78 and maturity index higher than 2 representing a well preserved forest environment with a rich complexity of micro- and macro- fauna and absence of soil disturbance events (Ferris and Bonger, 2006; Neher, 2001; Ferris et al., 2001;

Yeates et al., 1993). In the lab microcosms, nematodes from the transplanted core rapidly moved out and multiplied in large numbers (1500 bacteria feeding nematodes per 10g soil) utilizing the nutrients from the surrounding autoclaved soil. They spread in a 60cm X 60cm area within a short time period of 2 weeks after core transplantation and by weeks 4 and 5 higher trophic level nematodes

167 were also found at the largest sampling distance (20cm from core edge).

Comparison of the inoculum potential of the intact soil core with commercial topsoil in the field trial in turf grass plots, also gave similar results. This commercial topsoil had been exposed to heat and disturbances such as mixing and shoveling to mimic urban gardening practices. The core transplant treatment resulted in a significantly greater increase in the abundance of predatory and omnivorous nematodes in the surrounding soil, along with calculated nematode indices such as the structure index and the maturity index.

This technique is likely a highly effective method of enriching vacant lot soil biodiversity, since the core brings with it a structured and mature soil nematode food web along with other bacteria, protozoa, fungal spores, hyphae, collembola and arthropods, there are characteristic of a functionally diverse and mature forest ecosystem. At the same time it is not introducing any harmful plant parasitic nematodes or other herbivores that would endanger the food crops in community gardens, as was observed in the relatively steady plant parasitic index in the field trials. The same however cannot be said for procedures such as topsoil replacement where a truckload of soil brought in from an unknown source may bring along unwanted pests, parasites or a seed bank of invasive species in large quantities. The nutrient rich soil of the turf grass plots with an established community of the opportunistic r-selected species likely supported the introduction, growth and survival of the higher trophic levels in a short period of time (Hedlund et al., 2004).

168

However, soil ecosystem in vacant lots involves an additional variable that affects the soil food web diversity, i.e., a higher than background heavy metal concentration. Also, upon selection for conversion into a food garden, the common inputs in a conventionally managed community garden include water, organic matter, mulch, fertilizers, pesticides and herbicides. Most urban residents may not have access to farm produced cow, pig or chicken manure (De Bon et al.,

2008) and hence commercially produced organic compost is the common alternative. Topsoil brought in from a different farm to be used in raised beds also undergoes a large amount of disturbance, shoveling, mixing and exposure to heat that eliminates the sensitive higher trophic guilds. Addition of organic amendments can stabilize the metal concentrations in soil by binding them with humic acids (Erdogan et al. 2007). They may enhance the functioning of the soil food web by affecting the growth and responses of the resident microbial fauna

(Ferris and Matute 2003) however; they are rarely used for adding novel microbial populations to the soil.

Hence, the efficacy of core transplantation in introducing higher trophic guilds in vacant lots was analyzed in the Weinland Park neighborhood. The core transplant treatment was also accompanied by topdressing the soil with organic amendments differing in their C:N ratios i.e., compost (C:N of 12:1), grass clippings (20:1) and organic peat (25:1). Organic compost is rich in soil nutrients cations, C, N, can improve soil physical and chemical characteristics and increase microbial activity by providing readily consumable energy source for the resident

169 microbes (Brown and Cotton, 2011; Crecchio et al., 2001). Indeed, compost topdressing increased soil Ca, Mg and CEC values in the vacant lots. However, these commercially purchased organic amendments do not provide any additional faunal diversity to the soil ecosystem. The organic amendments were analyzed for their baseline nematode community composition and none were found to have any predatory nematodes while peat had very few omnivorous nematodes. Hence the conventional management practices in gardening do not enrich the faunal composition of the soil food web since there is no addition of a novel group of organisms originally missing from the vacant lot soil.

The lower C:N ratio of compost provided a labile source of carbon which resulted in the exponential growth of bacteria feeding nematodes and an increase in their numbers, while the high C:N ratio of peat was a suitable source of energy for fungus and fungus feeding microbes (Ferris and Matute, 2003). Different nematode feeding types dominate the soil food web depending on the composition of organic amendment used (Ferris and Matute, 2003). Additionally, predatory and omnivorous nematodes abundance increased in all the core transplanted plots as compared to the plots that did not receive any core, also translating into higher structure and maturity indices. Therefore, the intact core worked as an effective inoculum of the higher level trophic guilds in the urban vacant lots. Among all the core transplanted plots, core + organic compost as soil amendment showed the maximum increase in the abundance of OM and PR nematodes; closely followed by the core + grass and only core treatments. Thus showing that, conventional

170 urban agriculture management practices may provide nutrient enrichment to soil but are not sufficient for improving its microbial composition. Structure and complexity of the soil food web are essential for its functioning and they can be restored in vacant lots via fast and inexpensive core transplantations. One intact soil core successfully reintroduced the missing higher trophic guilds to an area of

2.32 m2 in a short time period of 4 weeks, after which large numbers of the higher trophic guilds were maintained for a time period of 8 weeks. Using organic amendments such as compost in conjunction with core transplantation can be used as an effective means of bringing back the pre-disturbance soil food web structure which included the presence of higher trophic guilds.

In conclusion, soil health and quality are the most important considerations for any vacant lot redevelopment initiative, especially for growing food crops. It is important to note that urban environments vary from one another in their soil physical and chemical characteristics and contaminant levels resulting in unique correlations between the abiotic and biotic components. Urban food garden management practices not only act as an important factor in establishing the future sustainability and yield potential from the food gardens, but also affect the soil physical, chemical and biological characteristics, as a lot transitions from an empty land parcel to a productive community food garden. Finally, use of an intact core is a fast and efficient method to reintroduce the missing links of the soil food web, much faster than using a different approach such as cover crops

171 which may take a few growing seasons to bring a change in the soil microbial community composition (Stirling et al., 2005).

This research has huge implications not just for urban agriculture but also for organic and transitioning agricultural practices for fast and inexpensive restoration of the multi-trophic interactions in soil food web. The method is not focused on the transfer of a single species, but involves the restoration of multiple taxa of beneficial soil flora and fauna. This is especially important when more sensitive species of nematodes, mites, ants and other collembolans may not be noticed as missing from the urban agricultural landscape. Their restoration back into the below ground soil biome will improve the derived ecosystem services potential, increase sustainability of urban food cropping, ultimately enhancing the social and economic well-being of the community.

My dissertation directly addresses the two major concerns of post- industrial cities all around the US, i.e., growing percentage of vacant land and increasing demand for food security in economically disadvantaged neighborhoods. It provides a means of efficient restoration of the empty land parcels as food gardens managed by local communities themselves, to improve their access to nutritional dietary requirements and becoming self-reliant. At the same time, my research emphasizes the use of an ecologically sound approach of transplanting intact cores that prevents large-scale disruption to multiple soil ecosystems.

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