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Below ground biological control in urban landscapes and assessment of factors influencing its

THESIS

Presented in Partial Fulfillment of the Requirements for the Degree Master of Science in

the Graduate School of The Ohio State University

By

Priyanka Yadav

Graduate Program in

The Ohio State University

2012

Master's Examination Committee:

Parwinder S. Grewal, Advisor

Casey W. Hoy

P. Larry Phelan

Mary Gardiner

Copyrighted by

Priyanka Yadav

2012

Abstract

The practice of urban has recently gained momentum due to its potential of making cities self-reliant and revitalizing disadvantaged neighborhoods enhancing food security, generating new employment opportunities and access to fresh fruits and vegetables. However, the suitability of urban soils for agricultural use is questionable given their highly disturbed and contaminated nature,. My research examined, the inherent biological control activity provided by urban soils and ways to enhance such this activity to support sustainable crop production. We quantified belowground biocontrol activity in urban gardens and vacant lots in three Ohio cities,

Columbus, Cleveland, and Akron, using an in-situ baiting technique. We hypothesized that belowground biocontrol services would differ between gardens and vacant lots and different biocontrol may be influenced by variation in structure characteristics of these sites. Biocontrol activity, as assessed by % mortality of baited , varied between 63% and 82% with higher activity often recorded in vacant lots compared with gardens. Major contributors of potential below-ground biological control activity were , followed by microbial and entomopathogenic , respectively. Ants showed higher % mortality in vacant lots than in urban gardens (p value = 0.04) whereas microbial pathogens exhibited higher mortality ii ingardens than vacant lots (p value = 0.002). Such substantial biological control activity is promising and suggests that enhancing this inherent biological control activity can substantially reduce agricultural inputs.

As the biocontrol organisms are sensitive to variations in management practices, we further studied these sites for soil health/quality characteristics so as to generate hypotheses regarding practices that will increase activity of these biocontrol organisms.

We found that potential biocontrol service by ants (as assessed by mortality of bait insect caused by ants) is associated negatively with enrichment index and NH4-N; and positively with number of nematodes and soil moisture. In contrast, mortality by microbes is positively associated with enrichment index, NH4-N, and negatively with the number of omnivore nematodes and soil moisture. Mortality by EPNs is associated positively with parasitic index, number of cp-1 class bacterial feeding nematodes, and negatively with combined maturity index, cp-2 class bacterial feeding nematodes and

NO3-N. Such site assessment for biocontrol agents and determining practices to enhance their activity in urban gardens will likely provide for a safe and sustainable control strategy to enhance the quality of food crops and environmental health. We expect that the results from this study can be integrated in establishment and management of urban gardens in Ohio and elsewhere and will contribute to improvements in human and environmental health.

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Acknowledgments

I wish to thank my adviser, Dr Parwinder Grewal, for intellectual support, encouragement, and enthusiasm which made this thesis possible, and for his patience in correcting both my stylistic and scientific errors.

I thank Dr. Dr. Casey W. Hoy, Dr. Larry Phelan and Dr. Mary Gardiner for stimulating discussions on the project, for providing the basic knowledge needed for designing the study and for guiding me through the statistical analysis of the study.

I am also grateful to all my lab members Dr. Zhiqiang Cheng, Dr. Ruisheng An,

Harit Bal and Kuhuk Sharma, and summer interns especially Kathy Duckworth for their support and help in the fieldwork.

Finally, I would like to thank Dr. Steven Naber for guiding me through the statistical analysis.

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Vita

1999……………………………India International School, New Delhi

2000-2006………………………Bachelor of Medicine and Bachelor of

Surgery, Gandhi Medical College, Bhopal, India

2007-2009…………………………Master of Science, Environmental Science,

The Ohio State University, USA

2009-2012…………………………Graduate Research/Teaching Associate,

The Ohio State University, USA

Publications

Priyanka Yadav, Woodbridge A. Foster, Timothy J. Buckley, William J. Mitsch,

Parwinder S. Grewal. Factors affecting mosquito populations in created wetlands - accepted in Urban

Yadav, P., Duckworth, K., Grewal, P.S., 2011. Habitat structure influences below ground biocontrol services: A comparison between urban gardens and vacant lots. Landscape and

Urban Planning. 104(2), 238-244.

Fields of Study Major Field: Entomology v

Table of Contents

Abstract...... ii

Acknowledgements...... iv

Vita...... v

List of Tables...... x

List of Figures...... xi

Chapters:

1. Introduction and literature review...... 1

1.1 ………………...... 1 1.1.1 Importance of urban agriculture...... 1 1.1.2 Issues and challenges faced in practicing urban agriculture...... 2 1.1.3 Strategic solution to the challenges………………………………….5 1.2 as soil health indicator………………………………...5 1.3 Nematode community indices ……………………………………………...…6 1.4 Natural biological control as a strategy...... 8 1.4.1 Why Belowground biological control...... 9 1.4.2 Belowground biological control agents...... 10 1.4.2.1 Ants………………………………………………………...10 1.4.2.2 /fungi………………………………………………11 1.4.2.1 Entomopathogenic nematodes……………………………..12 1.5 Rationale for the study…………………………………………………….…13 1.6 Specific objectives and hypothesis…...... 13 References…………………………………………………………..………..15

2. Belowground biological control activity in urban landscapes: A comparison between urban gardens and vacant lots ………………………………………………………...... 22

2.1 Abstract...... 22 2.2 Introduction...... 23 2.3 Materials and Methods...... 26 vi

2.3.1 Study sites…………………...... 26 2.3.2 Quantification of belowground biocontrol activity...... 28 2.3.3 Identification of the potential biocontrol organisms……………….30 2.3.4 Statistical analysis……………………………………………...... 31 2.4 Results...... 32 2.4.1 Total belowground biocontrol activity in urban gardens and vacant lots………………………………………………………………………..32 2.4.2 Relative contribution of different organisms to belowground biocontrol activity...... 32 2.4.3 Differences in total belowground biocontrol activity between newly established gardens and older gardens………………………………...... 33 2.4.4 Effect of cage type on biocontrol activity by different organisms…33 2.5 Discussion...... 34 References………………………………………………………………..…..41

3. Factors affecting belowground biocontrol activity...... 51

3.1 Abstract...... 51 3.2 Introduction...... 52 3.3 Methods...... 55 3.3.1 Study sites...... 55 3.3.2 Quantification of belowground biocontrol activity...... 57 3.3.3 Soil sample collection……………………………………………...58 3.3.4 Soil nematode extraction and identification……………………….58 3.3.5 Nematode community index calculation…………………………..59 3.3.5 Soil physical and chemical parameters…………………………….60 3.3.6 Data analyses………………………………………………………60 3.4 Results...... 61 3.4.1 Biological control in urban gardens and vacant lots of three Ohio cities: Cleveland, Akron and Columbus…………………………………61 3.4.2 Nematode community characteristics of urban gardens and vacant lots………………………………………………………………………..61 3.4.3 Soil physical and chemical characteristics in urban gardens and vacant lots of the Ohio cities: Akron, Cleveland and Columbus………...63 3.4.4 Nematode community characteristics and soil parameters affecting biological control activity………………………………………………..63 3.5 Discussion...... 65 References………………………………………………………………..…..70

Bibliography……………………………………………………………………………..87

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List of Tables

Table 2.1. Site locations and their Physicochemical Soil Characteristics……………….46

Table 3.1. F- and p-values from GLM ANOVA mixed/nested model on nematode community and soil property analysis for samples collected comparing community gardens and vacant lots in three cities of Ohio: Akron, Cleveland, and Columbus…..…82

Table 3.2. F- and p-values from GLM ANOVA mixed model on soil mineral analysis for samples collected comparing community gardens and vacant lots in two cities of Ohio:

Cleveland, and Columbus………………………………………………………………..83

Table 3.3. Regression coefficients giving the linear combination of standardized variables that compose the first two canonical axes in a canonical correspondence analysis of the relationship between mortality by different biocontrol agents and various biotic and abiotic soil quality/health variables in urban landscapes of three Ohio cities…………...85

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List of Figures

Figure 1.1. Graphic representation of the soil indicated by nematode faunal analysis (from Ferris et al., 2001). Bax (), Fux (fungivores), Cax

(, or predators), Omx () (where value of x = 1-5 on the cp scale) represents various functional guilds……………………………………………………….8

Figure 2.1. Percentage mortality of Galleria mellonella in urban gardens (UG) and vacant lots (VL) in Akron (2009) and Cleveland (2009 and 2010). Different letters on the bars indicate significant differences at p<0.05. ………………………………………...... 47

Figure 2.2. Percentage mortality of Galleria mellonella caused by different naturally occurring biocontrol agents in urban gardens and vacant lots over the two year study period in Akron and Cleveland. Different letters on the bars indicate significant differences at p<0.05……………………………………………………………………48

Figure 2.3. Percentage mortality of Galleria mellonella in urban gardens and vacant lots in Akron and Cleveland assessed by bait insects enclosed in cages with large (Cage 1) and small (Cage 2) mesh sizes. Different letters on bars indicate significant differences at p<0.05……………………………………………………………………………………49

Figure 2.4. Percentage mortality of Galleria mellonella caused by different naturally occurring biocontrol agents in urban gardens and vacant lots assessed by bait insects

ix enclosed in cages with large (Cage 1) and small (Cage 2) mesh sizes. Different letters on bars indicate significant differences at p<0.05…………………………………………..50

Figure 3.1. Percentage mortality of Galleria mellonella caused by different naturally occurring biocontrol agents in urban gardens and vacant lots over three year study period in Akron, Cleveland and Columbus, Ohio. Different letters on the bars indicate significant differences at p<0.05…………………………………………………………76

Figure 3.2. Nematode food web conditions in community gardens and vacant lots in

Akron and Cleveland, Ohio, USA………………………………………………………77

Figure 3.3. Total, free-living, and plant-parasitic nematode populations, and number of nematode genera in community gardens and vacant lots as well as in general in all the sites in Akron, Cleveland and Columbus, Ohio, USA. Data presented are Mean + SD.

Different letter(s) on bars indicate significant difference (p<0.05)……………………...78

Figure 3.4. Components of free-living nematodes: Bacteriovores (Ba), Fungivores (FF),

Omnivores (OM) and Predatory (PR) nematode populations in all the sites in Akron,

Cleveland and Columbus, Ohio, USA…………………………………………………...79

Figure 3.5. Nematode Structure Index, Enrichment Index, Maturity Index, Plant-parasitic

Index, and Combined Maturity Index in community gardens and vacant lots as well as in general in all the sites in Akron, Cleveland and Columbus, Ohio, USA. Data presented are Mean + SD. Different letter(s) on bars indicate significant differences (p<0.05)…...80

Figure 3.6. Total soil carbon (% C), pH, Magnesium, Phosphorus, Potassium and Cation exchange capacity in community gardens and vacant lots in Columbus, Cleveland, ±

x

Akron, Ohio, USA. Data presented are Mean +/± SD. Different letter(s) on bars indicate significant difference (p<0.05)…………………………………………………………..81

Figure 3.7. Canonical correspondence analysis of the relationship between mortality by different biocontrol agents and various biotic and abiotic soil quality/health variables in urban landscapes of three Ohio cities where the direction of arrows indicates correlation with the first two canonical axes and the length of arrows represents the strength of the correlations……………………………………………………………………………….84

Figure 3.8 Eigen values and percentages of inertia of the first three canonical axes (F1,

F2 and F3) from canonical correspondence analysis presented in the tabulated form and as a scree plot…………………………………………………………………………….86

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CHAPTER 1: INTRODUCTION AND LITERATURE REVIEW

1.1 Urban Agriculture

Urban agriculture goes beyond food production and includes activities like husbandry, , agro-forestry, and multipurpose wood production

(Mougeot, 1994). The Council on Agriculture, Science and Technology (CAST), defines urban agriculture incorporating all its aspects as “a complex system encompassing a spectrum of interests, from a traditional core of activities associated with the production, processing, marketing, distribution, and consumption, to a multiplicity of other benefits and services that are less widely acknowledged and documented. These include recreation and leisure; economic vitality and business entrepreneurship, individual health and well-being; community health and well-being; landscape beautification; and environmental restoration and remediation” (Butler and Maronek, 2002).

1.1.1 Importance of urban agriculture

Current economic downturn has caused ever increasing incidence of home foreclosures, unemployment and inner city poverty leading to hunger and malnutrition in

US urban neighborhoods. Urbanization further renders the urban population vulnerable to food insecurity by offsetting urban land against food production and creating high levels

1 of unemployment. According to a recent USDA-ERS report, 17.2 million households, which constitute 14.5 percent of households, were food insecure. About 13.5 million people live in food deserts and 13.9 million people were unemployed (USDA, 2011).

Further, although cities are growing at an unprecedented rate, they are mostly dependent on the ecosystems beyond the city limits for resources and services. With this challenge of urbanization coupled with current economic situation, urban agriculture has a potential of making cities self-reliant by providing required ecosystem services within the city limits. It has the potential to sustain cities by forming a closed-loop ecological system with urban dwellers as workers, using urban resources (vacant spaces, waste water and solid waste), and providing for urban consumers, thus having direct impacts on urban (positive and negative) (Nugent, 1999; RUAF, 2000). Thus, it can play a huge role in revitalizing affected neighborhoods by increasing availability of local and healthy produce and generating new employment opportunities in the production and marketing of that produce.

It can not only provide food security but also increase access to healthy and nutritious food (Minnich, 1983; Duchemin et al., 2008; Blaine et al., 2010), improve the environment (Doron, 2005; Flores, 2006), and promote a sense of community (Patel,

1991; Malakoff, 1995; Flores, 2006). It can also serve as a means to come close to nature that improves mental health and personal wellness along with providing opportunities for physical exercise (Brown et al., 2004; Brown and Jameton, 2000; Kaplan and Kaplan

1990; Malakoff, 1995).

1.1.2 Issues and challenges faced in practicing urban agriculture

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Urban agriculture may pose certain risks to health due to its associated disservices such as water contamination and use of partially treated waste. Composting for reusing solid organic waste reduces several health risks associated with improper waste disposal like transmission of diarrhea, increased breeding of mosquitoes, and contamination through scavenging (Zeeuw, 2000, Brown and Jameton, 2000). However, composting does not reduce the risk of heavy metal contamination and injury by non- biodegradable fragments present in the waste (Zeeuw, 2000, Jeevan and Shantaram,

1995; Nicolaisen et al., 1988). World Health Organization (WHO) and Polish researchers revealed that 60-80% of heavy metal toxins found in human bodies in urban industrial areas were the result of consuming contaminated foods rather than through air pollution

(Bellows, 1999). with improperly treated wastewater can also contaminate crops with pathogenic organisms (e.g. bacteria, protozoa, or helminths) and heavy metals (Zeeuw, 2000, Brown and Jameton, 2000). Chlorination of such wastewater effluent may further enhance the toxicity of the soil (Tarcher, 1992).

However, such harmful effects can be ameliorated by exercising precautions, public health initiatives and policy regulations. Simple safety measures on the can prevent injuries related to handling waste. Green leafy vegetables or tubers are more likely to absorb heavy metals from the soil than fruiting . Hence, in areas with heavily contaminated soils, preference should be given to cultivate fruiting plants.

Phytoremediation, i.e., growing plants that readily absorb heavy metals from the soil, can also be practiced. Standards of waste water and organic solid waste reuse need to be regulated strictly (Bellows et al., 2003).

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Another problematic issue comes from highly disturbed urban soils due to anthropogenic activities including compaction from heavy equipment use, removal of top soil, atmospheric deposition of toxic compounds, heavy metal contamination such as lead from paint and vehicle emissions, extensive fertilizer and chemical applications, use of de-icing salts, and other industrial contaminants (U.S. EPA 2004; Walsh 2000;

Lohse et al. 2008; Laidlaw, 2008). Such disturbances question the suitability of urban soils for food production. Urban agriculture may also create opportunities for new species to become established (Smith, 1990), e.g., pest species invading agroecosystems, probably due to the reduced natural enemy pressure and/or empty niche created by (Colautii et al. 2004; MacArthur 1970). This would further warrant increased reliance on fertilizers and pesticide inputs in these urban ecosystems which poses a significant health risk due to contamination of foodstuffs or ground water by residues of agrochemicals (fertilizers, & ) causing acute poisoning to long term organ impairments and chronic illnesses (WHO Commission on Health and Environment

1992; FAO and WHO 1988). Residues of agro-chemicals, sometimes far in excess of acceptable limits, are often found in red meat, poultry, locally grown vegetables and

(Forget, 1993; Conway and Pretty, 1991). However, such effects are preventable by practicing biological control or organic methods of cultivation.

An additional issue concerning urban agriculture is the availability of land due to with other land uses (Mougeot, 2006). However, urban land banks have expanded in US during the past few years due to increased home foreclosures (Grewal and Grewal, 2011) and, with proper diagnosis and management, urban agriculture can utilize these land vacancies productively. Thus, the challenge is to convert vacant land

4 into urban gardens without further degrading the soil and minimizing the use of agrochemicals.

1.1.3 Strategic solutions to the challenge

The strategic solutions will include the use and management of urban soils in a sustainable way. This would include:

Step 1 - Assessment and selection of each site by identifying the soil biological, physiochemical, nutritional and structural conditions.

Step 2 - Identifying soil management and pest management strategies that do not further degrade the soil.

In this project we propose to use nematodes and other soil organisms assemblages along with standard soil analyses for diagnosing soil conditions and evaluate natural activity provided by the .

1.2 Nematode community as soil health indicator

The assessment of soil quality or health is the primary indicator of sustainable land management (Karlen et al., 1997). A good indicator of soil quality and health should define ecosystem processes and integrate physical, chemical, and biological properties, should be sensitive to management and climatic variations, and should be accessible and easy to use (Doran and Parkin, 1996). These may include abiotic and biotic indicators however abiotic chemical, biochemical, and physical measurements usually describe the endpoint of ecosystem functions and processes unless they’re the result of human activity

5 whereas biotic indicators provide assessment of ecological change, stability, and sustainability of complex systems.

Nematodes can serve as of soil health/quality due to several attributes they possess. Nematodes are ubiquitous and most abundant metazoa inhabiting almost all ecosystems including marine, freshwater, and terrestrial environments (Yeates, 1979).

Soil nematodes indicate the biotic and functional status of soil food web due to their position in multiple (5-8) trophic levels including primary, secondary, and tertiary levels (Bongers and Ferris, 1999; Yeates et al., 1993). They are easy to isolate identify and classify. Classification is based on the morphology of the mouth cavity and pharynx which directly relates to their feeding habits enabling interpretation of their functions in soil. Nematodes respond rapidly to disturbance and enrichment, influence vegetation succession and indicate conditions in the soil horizon that they inhabit

(Bongers and Ferris, 1999).

1.3 Nematode community indices

Most of the soil nematode community indices are based on the functional concept. Functional guilds of soil nematodes are classified either by their feeding habits into bacteriovores, fungivores, omnivores, predators, and plant feeders, or by life-history strategy into colonizer-persister (cp) continuum of 1-5 (Bongers, 1990; Yeates et al.,

1993; Bongers and Bongers, 1998). Plant-parasitic nematodes are considered as primary consumers being (Ferris and Bongers, 2006). Bacteriovore and fungivore nematodes feed on such as bacteria and fungi significantly contributing to nutrient mineralization (Ferris and Matatue, 2003; Ferris et al., 1996; Ingham et al., 1985;

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Ferris et al., 2004). Predatory nematodes regulate the food web by preying on nematodes and other invertebrates in the soil (Grewal et al., 2005). c-p value 1 nematodes are short lived, have high fecundity, and respond rapidly to available nutrient flush, while c-p value five nematodes are large in size, have longer life span, low fecundity, are susceptible to disturbance and are predominantly omnivores and predators (Bongers,

1990). The Maturity index (MI) is calculated as the weighted mean frequency of the cp classes and assesses soil disturbance, enrichment, and nematode community succession

(Bongers, 1990; Neher, 1999). Ferris et al. (2001) devised enrichment (EI) and structure

(SI) indices by assigning weights to indicator nematode guilds representing basal, enriched and structured conditions of the soil food web. The EI indicates the abundance and activity of primary detrital consumers and describes whether the soil condition is nutrient enriched or depleted. The SI weighs high cp nematode guilds that require environmental stability for population growth and hence indicates the degree of maturation of the soil nematode food web with greater trophic links indicating structured system and fewer trophic links indicating degraded system. EI and SI can be plotted to provide a model framework of nematode faunal analysis which serves as an indicator of the likely conditions of the soil food web (Figure 1.1).

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Figure 1.1. Graphic representation of the soil food web indicated by nematode faunal analysis (from Ferris et al., 2001). Bax (bacterivores), Fux (fungivores), Cax (carnivores, or predators), Omx (omnivores) (where value of x = 1-5 on the cp scale) represents various functional guilds. Indicator guilds of soil food web condition (basal, structured, enriched) are designated and weightings of the guilds (numbers in parenthesis) along the structure and enrichment trajectories are provided, for determination of the enrichment index (EI) and structure index (SI) of the food web.

1.3 Natural biological control as a pest control strategy

Biological control has been defined as the “study, importation, augmentation, and conservation of beneficial organisms to regulate population densities of other organisms”

(DeBach 1964). These beneficial natural enemies include predators, pathogens and . In this project we studied aspects of conservation biological control which implies environmental modification to protect and enhance natural enemies (DeBach

1964). We seek to understand resident natural enemies in urban ecosystems and factors influencing them in order to suggest measures to enhance the ability of natural enemies to suppress pests.

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Enhancement of natural biological control has been suggested as a prime preventive tactic for pest management in recent literature (Isaacs et al., 2009; Letourneau and Bothwell, 2008; Schellhorn et al., 2008). However, only a few studies have addressed the level of pest control offered by integral natural enemy complexes in urban landscapes.

Most of the studies were conducted in large scale agroecosystems or turfgrass ecosystem.

Rice fields in tropics are being effectively managed by conserving natural generalist predators with minimal chemical inputs (Settle, 1996). Though agricultural systems are thought of as disturbed and evolutionarily recent managed ecosystems, rice fields are known to exist from 9000 yrs (Bray, 1986) and so have a long ecological history of co- existing stable natural enemy populations. However, some newly established soybean agroecosystems have also exhibited effective control by inherent biological control agents (Liu et al., 2004; North Central Soybean Research Program, 2008). Lopez and

Potter (2000) showed that the Lasius niger preyed heavily on black cutworm eggs and first instars and Japanese eggs, and the was lower in golf course fairways than in roughs. Also fewer grubs were found in areas where ants were abundant than where ants have been controlled by . Similar studies on turfgrass ecosystem suggest that natural enemies help suppress populations of turfgrass insect pests (Zenger and Gibb, 2001; Braman et al. 2002, 2003; Rogers and Potter, 2004b). These studies are promising because they implicate that biocontrol agents are effective and could be further enhanced or conserved to substantially reduce the need for chemical inputs.

1.4.1 Why belowground biological control

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To date, the majority of studies have examined the complex interactions of existing natural enemies occurring above ground.These biological control interactions are often difficult to manipulate as they are affected by multiple above as well as below ground abiotic and biotic factors. Additionally, urban agriculture mainly concerns vegetable production and several important pests are either soil insects or have soil dwelling stages as pests, e.g. cutworm, wireworms, grubs, armyworms, etc (Trumble

1994). Below ground natural enemies can prey on soil-dwelling stages (eggs, larvae, pupae and adults) of such diverse insect pests often reducing the frequency and intensity of pest outbreaks (Cockfield and Potter, 1984; Grewal, 2012; López and Potter, 2000;

Potter, 2005).

1.4.2 Belowground biological control agents

The major biocontrol activity in the soil foodweb is provided by predators like ants, microbial pathogens, and by entomopathogenic nematodes (reviewed by Denno et al., 2008).

1.4.2.1 Ants

Ants (Formicidae) are the most widely distributed and abundant social insects.

Ants have been identified as one of the major generalist predators and ecosystem soil engineers due to their ability to suppress pest activity and cause physical changes in biotic and abiotic materials thus directly or indirectly affecting other species (Way, 1992;

Jouquet, 2006). Ants can change the soil conditions by affecting soil texture, chemical composition of various elements like C, P, N and K and microbial and microfaunal

10 communities through their various activities like food storage, accumulation of feces, corpses and food remains (reviewed by Cerda and Dejean, 2011). Except for some ground-nesting and ground- species acting as strictly predators, most ant species are generalist feeders. These predatory soil-dwelling ant species prey on invertebrates or including earthworms, acarids, isopods, different kinds of myriapods (e.g., iulids, chilopods, polyxenids), collembolans, , , bark lice, epidopterans, etc. They can significantly decrease the size of potential populations justifying their potential use for biological control purposes (Rico-Gray et al., 2007). Some other attributes that make ants biological control agents include their ability to remain abundant even when prey is scarce as they can use other stable sources of energy like their own brood and insect/plant exudates; their ability to store food and hence continue predation even if not needed instantly; their ability to deter larger herbivores thus increasing their activity range; and the ease of being managed to enhance their abundance, distribution, and contact with prey (Rico-Gray et al., 2007).

1.4.2.2 Bacteria/fungi

Soil bacteria and fungi are major components of the soil food web. They serve as indicators of soil quality/health and provide suppression of many insect pests in agroecosystems (Kennedy, 1999; Knudson, 2006; reviewed by Doran and Zeiss, 2000).

Microbes may exhibit biological control activity through , competition, or production of plant growth promoting compounds (Klopper 1992). The success in use of microbes as biological control agents against many pests including pathogenic fungi has been widely studied and accepted (Grewal, 1999; Weller 1988;

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Byer and Sikora 1990; Bhatt and Singh, 2002). One of the reasons why bacteria and fungi are considered indicators of soil quality is their sensitivity to variations in land management practices (Wu et al., 2008; Bulluck and Ristaino, 2002; Degens et al., 2001).

This property may be utilized to manipulate communities of beneficial bacteria and fungi to enhance natural pest control in urban gardens.

1.4.2.1 Entomopathogenic nematodes (EPNs)

Entomopathogenic nematodes (EPNs) belong to families Steinernematidae and

Heterorhabditidae and have been known to suppress populations of pest insects in a variety of agroecosystems (Lewis et al., 1998; Mracek, 2002; Barbercheck & Hoy, 2005;

Georgis et al., 2006). The parasitic stage is the third free-living juvenile stage known as the infective juvenile (IJ).They enter through the host insect's natural body openings like the mouth, anus or spiracles and in some cases through inter-segmental membranes of insect cuticle by using an anterior tooth finally penetrating into the blood cavity from the gut (Poinar, 1990; Bedding & Molyneux, 1982). In the blood cavity of the host insect, they release a highly specialized symbiotic bacterium ( spp. in Steinernema,

Photorhabdus spp. in Heterorhabditis) which multiply and rapidly kill the insect within a day or two (Akhurst & Bedding, 1986).

EPNs are ubiquitous occurring widely in natural and agreoecosystems, and are generalized predators of insects in soil food webs. They are compatible with Integerated pest management (IPM) programs particularly for soil pests (Grewal et al., 2005; Grewal,

2012). Successful activity of EPN activity has been documented against a broad range of insect pests like white grubs, , northern masked chafer, cutworms,

12 webworms, billbugs, mole crickets, peach borer , carpenter worm, , scarabs, etc. with no effect on non-target organisms (Georgis et al., 2006; Grewal et al.,

1998;2005; 2012). Commercial application of EPNs has been successful against soil insects as well as against some above-ground insects (Arthers et al., 2004; Shapiro-Ilan et al. 2006). The attributes that make EPNs a good biological control agent include their wide host spectrum, active host seeking behavior, ability to kill the host within 48 h, easy mass production, long-term efficacy, easy application, compatibility with most chemicals, and environmental safety (Poinar, 1990; Kaya, 1990).

1.4 Rationale for the study

The focus needs to be on minimizing the risks associated with urban agricultural practices. The approach of converting vacant lands to healthy urban gardens requires identifying biological and physiochemical soil characteristics to begin with. Different strategies are then required to increase the quality of soils in new and established urban food gardens. This project looks at the health of the soil food web and biocontrol services provided in the urban soils which is one of the required initial steps. Furthermore, assessment of the factors that affect biocontrol agents and their activity can assist in determining practices to enhance their activity in urban gardens which will provide for a safe and sustainable pest control strategy to enhance the quality of food crops and environmental health.

1.5 Specific objectives and hypothesis

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Overall goal of this study was to assess the potential and existing urban garden sites for soil quality/health & existing below ground biocontrol activity, and to assess the factors that influence below ground natural biocontrol activity so as to generate hypotheses regarding practices that could enhance below ground natural biocontrol activity.

Objective 1: Determine below ground biological pest control activity provided by the soil food web in urban landscapes

Hypothesis 1. Below ground biocontrol activity will differ among urban sites due to diverse habitat structure and management intensity

Objective 2a: Assess soil quality and food-web health in urban landscapes to quantify disturbance and look at the possible patterns and correlation with biocontrol activity

Objective 2b: Generate hypotheses regarding practices that could enhance below ground biocontrol activity

Hypothesis 2. Belowground biocontrol activity will positively correlate with the health of the soil food web and soil quality

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References

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Arthurs, S., Heinz, K.M., Prasifka, J.R., 2004. An analysis of using entomopathogenic against above-ground pests. Bull. Entomol. Res. 94, 297–306.

Bakker, N., Dubbeling, M., Guendel, S., Sabel Koschella, U., de Zeeuw, H., 2000. Growing Cities, Growing Food : Urban Agriculture on the Policy Agenda: A Reader on Urban Agriculture. Leusden (The Netherlands): Centre on Urban Agriculture and Forestry (RUAF).

Barbercheck, M.E., Hoy, C.W., 2005. A systems approach to conservation of nematodes, in: Grewal, P.S., Ehlers, R.U., Shapiro-Ilan, D.J. (Eds.), Nematodes as Biocontrrol Agents. CABI Publishing, Wallingford, UK, pp. 331- 348.

Bhatt, N., Singh, R.P., 2002. Casing soil bacteria as biocontrol agents against the mycoparasitic fungi of Agaricus bisporus. Proceedings of the 4th International Conference on Mushroom Biology and Mushroom Products. 1-9.

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CHAPTER 2: BELOWGROUND BIOLOGICAL CONTROL ACTIVITY IN URBAN

LANDSCAPES: A COMPARISON BETWEEN URBAN GARDENS AND VACANT

LOTS

2.1 Abstract

Urban agriculture offers a framework for local self-reliance by provisioning food security, employment opportunities, and other community benefits. However, urban agriculture must rely on the supporting and regulating services of the soil food web.

Hence, we quantified belowground biocontrol activity in urban gardens and vacant lots in two post-industrial cities using an in-situ insect baiting technique. Due to the differences in habitat structure, we hypothesized that belowground biocontrol services will differ between gardens and vacant lots and the influence of habitat structure would differ with the type of biocontrol . Results revealed that biocontrol activity, as assessed by

% mortality of baited insects, varied between 51% and 98% with higher activity often recorded in vacant lots than gardens. Major contributions to bait insect mortality were by ants, followed by microbial pathogens and entomopathogenic nematodes, respectively.

Ants showed higher (p < 0.0001) % mortality in vacant lots (60% ± 33.4%) than in urban gardens (33.3% ± 22.2%) whereas microbial pathogens exhibited higher (p < 0.0001) mortality in gardens (27.8% ± 15%) than vacant lots (8.3% ± 16.7%). Ants caused higher

(p< 0.0001) mortality when larger-mesh size cages were used compared with the smaller-

22 mesh size cages, but mortality by microbial pathogens did not differ with cage type. The high biocontrol activity indicates the resilience of the soil food web in urban ecosystems and the differential effects of habitat structure on biocontrol activity can help guide landscape planning and vegetation management to enhance urban environments and boost local self-reliance.

2.2 Introduction

Urban agriculture offers a comprehensive framework for local self-reliance and resilience and a means to reducing the of cities (Grewal and Grewal,

2011). Interest in urban agriculture has escalated recently due to the accumulation of vacant land particularly in post-industrial U.S. cities (Callis and Cavanaugh, 2008) and motivation to address food insecurity and childhood obesity issues in disadvantaged urban neighborhoods. Urban agriculture can revitalize affected cities and neighborhoods by generating new employment opportunities, increasing access to healthy food and sustaining cities by forming closed-loop ecological systems with vacant spaces, waste water and solid waste as potential resources (Lorenz and Lal, 2009; Nugent, 1999).

Indeed North American cities have the necessary resources to substantially increase their self-reliance in fresh produce and reduce local economic leakage (Grewal and Grewal,

2011). However, urban soils are highly disturbed due to anthropogenic activities such as compaction by heavy equipment, removal of top soil, atmospheric deposition of toxic compounds, heavy metal contamination, extensive fertilizer and chemical pesticide applications, de-icing salts, and other transport and industrial contaminants (Lohse et al.,

2008; Pouyat et al., 2010) and pose a threat to biodiversity (McDonald et al., 2008;

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Puppim de Oliveira et al., 2011). An important regulatory ecosystem service associated with biodiversity is natural pest control (Gurr et al., 2003) which can enable sustainable crop production (Naylor and Ehrlich, 1997; Ostman et al., 2003) without reliance on the use of toxic chemical pesticides. Hence, conserving natural pest and disease control services of the soil food web is crucial for minimizing human and environmental exposure to chemical pesticides and for enhancing local self-reliance through ecological design of urban ecosystems.

The natural enemy complex including predators, parasitoids, and pathogens have the potential to regulate pest populations and become a central part of integrated pest management strategy (Kogan, 1998). Enhancement of natural biological control has been suggested as a prime preventive tactic for pest management in recent literature (Isaacs et al., 2009; Letourneau and Bothwell, 2008; Schellhorn et al., 2008). However, studies on the occurrence of natural biological control agents and the extent of pest control services they render in urban soils are sparse. Additionally, due to differences in functional processes acting on fragmented landscapes (Byrne and Grewal, 2008; Pickett and

Cadenasso, 2008), in depth ecological studies addressing small scale urban parcels/patches are needed.

We focused on belowground generalist biocontrol agents including ants, microbes and entomopathogenic nematodes which prey upon soil-dwelling stages of diverse insect pests affecting urban agriculture. Ant communities in urbanized ecosystems have been found to be vulnerable to urban development, fertilization and other vegetation management practices and occurrence of human/animal/vehicle traffic (Clarke et al.,

2008; Gotelli and Ellison, 2002; Lassau and Hochuli, 2004; Sanford et al., 2009). Though

24 these studies have addressed and abundance, the extent of biocontrol service provided has not been studied. Also few studies have addressed the effect of land use change on microbial communities. Diquelou et al. (1999) found that microbial activity tends to decline several years after establishment of agriculture. Scharenbroch et al. (2005) found that old residential landscapes had higher microbial than new residential landscapes most likely due to greater time since disturbance. Similarly, Park et al. (2010) found that soil nematode food webs were relatively more structured in older parts of the cities than the more recently developed areas on the urban fringe. Though these studies show the influence of anthropogenic activities on the structure and diversity of invertebrate and microbial communities, enhanced understanding of pest regulation services they provide is critical for designing ecologically-based cultural practices for urban agriculture.

Therefore, the main aim of this study was to assess the extent of naturally occurring belowground biological pest control services in post-industrial cities which have accumulated substantial amounts of vacant land. We used an in-situ baiting technique to quantify biocontrol activities in community gardens and vacant lots provided by the major groups of biocontrol agents known to provide belowground pest regulation services (Denno et al., 2008). As habitat structure, defined as the composition and arrangement of physical matter (Byrne, 2007), can regulate community structure by providing resources (shelter, nutrients, nesting sites) and mediating interactions (e.g. predation, competition) for a diverse array of organisms in many ecosystems (Bell et al.,

1990; Byrne, 2007; Tews et al., 2004), we tested if human modification of habitat structure would influence belowground biocontrol services rendered by invertebrate and

25 microbial communities. Because habitat structure can differ considerably between urban gardens and vacant lots, we hypothesized that these two land covers would differ in the extent of belowground natural biocontrol services and the influence of habitat structure would differ with the type of biocontrol agent. Specifically, we hypothesized that vacant lots (which are left unmanaged following building demolition except for occasional mowing to keep the vegetation height short) would exhibit higher belowground biocontrol activity than urban gardens which possess heterogeneous, sparse, and relatively taller plant species and receive regular tillage, irrigation, weeding, and chemical fertilizer and pesticide inputs. The percentage mortality of the model bait insect was used as an index for biocontrol service/activity. We also hypothesized that ant predation would be more in vacant lots due to permanent ground cover with greater structural complexity, lower moisture content and minimal disturbance compared to gardens, whereas the reverse would be true for microbial pathogens which require high relative humidity and soil moisture for persistence and optimal activity.

2.3 Methods

2.3.1 Study sites

Twenty two urban gardens and twenty three vacant lots were studied for belowground biological insect control services provided by soil invertebrates and microorganisms over a two year period in two post-industrial Ohio cities, Akron (41

05’05’’N, 81 30’56’’W) and Cleveland (41 29’58’’N, 81 41’37’’W). The two cities have average monthly temperatures of -4°C in January and 22°C in July and average annual precipitation of 91.9 to 101.3 cm. We identified six community gardens and six nearby

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(within 1 mile) vacant lots in Akron and seven urban gardens and seven nearby vacant lots in Cleveland for sampling during July and August in 2009. Additionally, nine new community gardens and ten new vacant lots in Cleveland were studied in July and August in 2010. The community gardens in Akron were established only in 2009 (i.e. were only

3-4 months old), whereas those in Cleveland were much older (the majority being 15-30 years old). We used the word ‘vacant lot’ to represent the larger urban context for these spaces from which houses had been demolished and the building footprint had been re- colonized by natural and weedy species over time.

Site addresses, soil texture, soil pH and % organic matter for all gardens and vacant lots are given in Table 2.1. In general, soil texture and pH conditions varied substantially but randomly in urban gardens and vacant lots of Akron and Cleveland. Soil organic matter however, tended to be higher in urban garden sites as compared to vacant lots most likely due to amendments.

These community gardens and vacant lots differed in two key components of habitat structure: heterogeneity and complexity. The gardens were more heterogeneous with respect to composition and arrangement of vegetation than the vacant lots, whereas vacant lots had more complexity than gardens in the volume and numbers of distinct leaves of grassy and weedy species. The commonly planted species of vegetables and fruits in the community gardens were: Solanum lycopersicum (tomato), Solanum tuberosum (potato), Daucus carota (carrot), Cucurbita pepo (zucchini), Cucurbita mixta

(pumpkin), Lactuca sativa var. longifolia (romaine ), Capsicum annuum (bell pepper), Cucurbita moschata (squash), Phaseolus vulgaris (beans), oleracea

(cabbage), Brassica oleracea (broccoli), Rubus idaeus (raspberry), Vitis vinifera (),

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Spinacia oleracea (spinach), Pisum sativum (pea), Brassica oleracea var. acephala (cole),

Citrullus lanatus (watermelon), Cucumis melo (cantaloupe), Mentha sachalinensis

(mint), Brassica oleracea (cauliflower), Prunus avium (cherry), Raphanus sativus

(radish), Zea mays (maize), Allium sativum (garlic), Helianthus annuus (sunflower),

Solanum melongena (eggplant), and Ipomoea batatas (sweet potato). Most of these species were found in most gardens except for raspberry, grape, cherry and mint being found in fewer gardens. As expected these annual species were planted in distinct patches with only a few sparsely planted individuals of a single species per patch. The gardens were also regularly tilled, weeded, and irrigated but had no pesticide inputs except for occasional fertilizer applications.

In contrast, the vacant lots were typically covered in grassy and weedy species and were occasionally mowed to look like urban lawns. Twenty of the 23 vacant lots were predominantly covered in turfgrass and associated weedy species such as Poa annua (annual bluegrass), Digitaria ischaemum (smooth crabgrass), Festuca arundinacea

(tall fescue), and Taraxacum officinale (dandelion), and appeared to be mowed frequently. Two vacant lots in Akron were predominantly covered with weedy species, including Trifolium pratense (red clover), Plantago lanceolata (plantain), Trifolium repens (white clover), Dactylis glomerata (orchardgrass), Daucus carota (wild carrot), and Cichorium intybus (chicory), and also appeared to be mowed occasionally. Finally, one vacant lot in Akron was wooded with trees including Acer saccharum (sugar maple),

Populus deltoides (cottonwood), and Quercus rubra (red oak); however, at the ground- level majority of the site was still grassy and weedy like the other sites, and appeared to be occasionally mowed.

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2.3.2 Quantification of belowground biocontrol activity

In order to quantify the insect biocontrol services provided by the naturally occurring belowground organisms, an in-situ baiting technique (Bedding and Akhurst,

1975) was used with the last instar wax moth Galleria mellonella larvae as bait insects.

G. mellonella are routinely used as model systems for detecting insect antagonists present in soil (Baur et al., 1998; Vanninen, 1995; Zimmermann, 1986). Each garden or vacant lot site was divided into three approximately equal sections for the 2009 study and four equal sections for the 2010 study. Six equally spaced locations were chosen (depending on the size of the site) on a linear transect in each section for burying the bait insects. We used this systemic (grid) sampling was conducted to account for unknown and discrete in-plot variability in both vacant lots and urban gardens. In 2009, a hand-made wire mesh cage (4 x 4 x 1 cm; mesh size = 16) containing three last instar G. mellonella larvae was buried 10-15 cm below the soil surface at each of the six locations on the transect. The cages were used to hold bait insects in place to allow for predation by belowground biocontrol agents but exclude larger aboveground predators including rove beetles, centipedes, , and skunks, etc. However, as we observed a very high level of predation by ants, we also used smaller-mesh size cages in 2010 to determine if high ant predation affected larval infection with relatively ‘slow acting’ microbial pathogens.

These smaller-mesh size cages, obtained from Qualityfilters Inc., were steel wire mesh tubes (10 cm long by 3 cm dia with mesh size = 24) which were also buried at each of the six locations on the transect, about 30 cm away from the hand made cages. Four G. mellonella larvae per cage (both small and large-mesh sizes) were used in 2010. Cages

29 were filled with soil from the site before placing them in the ground to ensure contact between G. mellonella larvae and the soil.

In total 1380 cages (468 cages in 2009 and 912 cages in 2010) were buried in all sites combined. All the cages were recovered after two days and brought to the laboratory in ice coolers (Bedding and Akhurst, 1975). This baiting duration was chosen to minimize natural larval mortality, enable early recognition of symptoms of infection, and to avoid a complete loss of baited insects due to predation or bacterial liquification. The G. mellonella larvae were sorted as dead or alive and all living larvae were observed for two additional days to record any additional mortality and signs of pathogen infection. The total numbers of dead larvae in each plot were recorded and the potential cause of mortality was determined using symptoms exhibited by the cadavers as described below. To assess control mortality (estimation of any natural death of the larvae) and to witness signs of late EPN infection, three sets of ten larvae from same G. mellonella batch were kept in 10 cm dia Petri dishes lined with wet filter papers at room temperature in the laboratory for four days and the numbers of live and dead larvae were recorded.

2.3.3 Identification of the potential biocontrol organisms

The death of each G. mellonella larva was attributed to a pathogen or predator based on physical condition, color, hardness and smell of the cadaver (Tanada and Kaya,

1993). If the cadaver was partially eaten, had dark spots on the body, had a hard texture and no pungent smell, it was considered to be killed by ants. Ants were often found in the cages showing the above described symptoms further supporting the potential cause of

30 death. If the cadavers were light brown to black, gave off an offensive smell and were hard or soft, they were presumed to be killed by bacteria or fungi. If the cadavers turned red to brown in color, were soft and gave off no foul smell, they were considered to be killed by entomopathogenic nematodes (Tanada and Kaya, 1993). Cadavers exhibiting signs of nematode infection were placed on White traps (White, 1927) to collect emerging infective juveniles which were identified using morphological characteristics described by Nguyen and Hunt (2007) for further confirmation of infection by entomopathogenic nematodes.

2.3.4 Statistical analysis

All G. mellonella larval responses were measured as binary variables. Proportion of larvae killed in each section of each site was recorded as percentage (%) larval mortality by pooling data from all the six locations on the transect in that section. The percentage mortality data were used as an index of biocontrol activity. Since there was no control mortality of G. mellonella we did not correct for control mortality. Percentage mortality of G. mellonella caused by different biocontrol agents individually was also recorded for each sub-site. Percentage data were rank transformed and then subjected to

ANOVA with the General Linear Model Procedure (GLM) with transformed means compared with Tukey’s Significant Difference Test. Type of site (urban garden vs vacant lot), city (Akron Vs Cleveland), age of urban garden (new vs old) and cage type (large mesh Vs small mesh) were included as categorical fixed factors in the model along with relevant interaction terms. Analysis was carried out separately for each year data initially.

As no difference was seen between the two years in Cleveland plots, the data were

31 combined to represent a single sample. Differences were considered significant at p ≤

0.05 and all data were analyzed using Minitab Release 16 (Minitab Inc., State College,

PA).

2.4 Results

2.4.1 Total belowground biocontrol activity in urban gardens and vacant lots

Total natural belowground biocontrol activity as assessed by % mortality varied between 51% and 98% at the studied urban gardens and vacant lots. Though significant differences between urban gardens (mean mortality 75% ± 20%) and vacant lots (mean mortality 87% ± 19%) were observed (p = 0.021; GLM), post hoc comparison was only significant between Cleveland vacant lots surveyed in 2010 and Akron urban gardens surveyed in 2009 (p = 0.005; Tukey’s test) (Figure 2.1). When examined separately for each city and year, the total % mortality did not differ significantly between urban gardens and vacant lots (p = 0.8 for Akron 2009; p = 0.9 for Cleveland 2009 and p = 0.36 for Cleveland 2010; GLM) (Figure 2.1). We also compared % mortality in Cleveland plots between 2009 and 2010 surveys and found no significant differences in overall bait insect mortality in urban gardens (p = 0.9; GLM) or vacant lots (p = 0.9; GLM) between the two years of study (Figure 2.1).

2.4.2 Relative contribution of different organisms to belowground biocontrol activity

Ants and microbes (bacteria and fungi) contributed most to belowground biocontrol activity, whereas entomopathogenic nematodes showed minimal activity in both urban gardens and vacant lots (Figure 2). Ants provided significantly higher %

32 mortality (60% ± 33.4%) than microbes (8.3% ± 16.7%) in vacant lots (p < 0.0001;

GLM) but there were no differences (33.3% ± 22.2% by ants vs. 27.8% ± 15% by microbes) in urban gardens (p = 0.99; GLM) (Figure 2.2). Overall, ants caused higher % mortality of the bait insects in vacant lots than in urban gardens (p-value = 0.0004;

GLM). Comparison of % mortality by microbes in urban gardens versus vacant lots revealed significantly higher mortality in urban gardens (p-value < 0.0001; GLM).

Percentage bait insect mortality caused by nematodes varied between 0 and 3.1% and did not differ between urban gardens and vacant lots (p-value = 0.99; GLM). The nematodes were identified to the level with 71.5% of the nematode-induced insect mortality caused by Steinernema and 28.5% by Heterorhabditis.

2.4.3 Differences in total belowground biocontrol activity between newly established gardens and older gardens

We compared urban gardens in Akron, which were established within one year of our study, to urban gardens in Cleveland which were 5-50 years old. As we did not find any significant difference in overall mortality between the Cleveland 2009 and 2010 plots, we considered these plots as one sample and compared it to Akron plots. Overall,

Akron urban garden sites exhibited relatively lower level of natural biocontrol as expressed by mortality of G. mellonella (67% ± 15%) than Cleveland sites (78% ± 18%), but the difference was not significant (p = 0.14; GLM). Similarly, % mortality in vacant lots between Akron (74% ± 31%) and Cleveland (94% ± 17%) did not differ significantly

(p = 0.15; GLM).

33

2.4.4 Effect of cage type on biocontrol activity by different organisms

Total % bait insect mortality was significantly less (p < 0.0001; GLM) when cages with smaller mesh sizes (mesh size = 24) were used compared to cages with larger mesh sizes (mesh size = 16). Mean mortality of baited larvae when using cages with larger mesh sizes in urban gardens was 75.0% ± 20.8% as opposed to 51.4% ± 29.5% for cages with smaller mesh sizes (Figure 2.3). For vacant lots, similar lower representation of mortality was evident for cages with smaller mesh sizes (35.4% ±27.5%) compared to cages with larger mesh sizes (80.8% ± 25.8%) (Figure 2.3). We also analyzed individual differences for the representation of mortality by different biocontrol agents and found significant difference in mortality caused by ants (more in cages with larger mesh sizes than cages with smaller mesh sizes, p < 0.0001; GLM) but no differences in larval mortality by microbes or nematodes in either cage (Figure 2.4).

2.5 Discussion

Besides being key mediators of soil functions, soil organisms provide one of the most important ecosystem services, controlling pests and pathogens (Lavelle et al., 2006).

Belowground natural enemies can prey on soil-dwelling stages (eggs, larvae, pupae and adults) of diverse insect pests in low maintenance urban lawns, often reducing the frequency and intensity of pest outbreaks (Cockfield and Potter, 1984; Grewal, 2011;

López and Potter, 2000; Potter, 2005). This two year study of urban gardens and vacant lots in two post-industrial cities shows that all the sites had high belowground natural biocontrol activity as indicated by 51-98% mortality of insects baited in the ground. We partitioned the relative contribution of different soil invertebrates and microbes to the

34 overall biocontrol service in these urban ecosystems. Ants and microbial communities contributed a majority of the biocontrol service, with ants exhibiting significantly higher biocontrol activity than microbes particularly in vacant lots. Lopez and Potter (2000) showed that the ant Lasius niger preyed heavily on black cutworm (Agrotis ipsilon) eggs and first instars and Japanese beetle (Popillia japonica) eggs, and the predation was lower in golfcourse fairways than in roughs. Fewer grubs were found in areas where ants were abundant than where ants have been controlled by insecticides. Ants have been identified as one of the major generalist predators and ecosystem soil engineers due to their ability to suppress pest activity and cause physical changes in biotic and abiotic components, thus directly and indirectly affecting other species (Jones et al., 1997;

Jouquet et al., 2006; Way and Khoo, 1992). Soil bacteria and fungi, on the other hand, are major components of the food web, serving as indicators of soil quality and health, and providing suppression of many insect pests in agroecosystems (Doran and

Zeiss, 2000; Knudsen, 2006) and urban lawns (Potter, 2005; Grewal, 2011). Our findings support the potential significance of ants and microbial communities to the provision of insect biocontrol services in urban landscapes. Also the high levels of belowground biocontrol activity in vacant lots and urban gardens observed here could serve as a foundation for building sustainable pest management practices for urban agriculture in cities.

The observed differences in the level of belowground biocontrol services in the two land use types appear to relate well to the differences in the essential components of habitat structure (heterogeneity and complexity) between urban gardens and vacant lots.

Results showed that belowground biocontrol activity was often higher in vacant lots than

35 in urban gardens. While gardens had higher heterogeneity with respect to composition and arrangement of vegetation than the vacant lots, they had lower complexity than vacant lots in the volume and numbers of distinct leaves of grassy and weedy species.

Byrne (2007) defined habitat structure as the amount, composition and three-dimensional arrangement of biotic and abiotic physical matter within a defined location and time.

Urban garden sites used in the study had annual species of fruits and vegetables planted in discrete patches, whereas vacant lots were almost uniformly covered by one or two turfgrass grass species and several other grassy and weedy species. The average vegetation height was approximately 15 to 45 cm in the gardens whereas it was maintained at 8 to 10 cm by mowing in the vacant lots. The 2009 Akron and Cleveland gardens and vacant lot sites used in this study were also investigated for soil physical, chemical and biological characteristics by Grewal et al. (2011). They found that urban gardens had higher soil moisture, organic matter, and nitrate-nitrogen as compared to the vacant lots, however nutrient availability and nutrient cycling as assessed by microbial biomass, rate, and nematode community enrichment index were not different between the gardens and vacant lots (Grewal et al., 2011). They concluded that these differences were most likely due to the inputs of water (irrigation), compost, fertilizer, and tilling in urban gardens compared to vacant lots which did not receive these inputs. All the urban garden sites used this study were regularly tilled, weeded, and irrigated but had no pesticide inputs except for an occasional fertilizer application. These differences in inputs and disturbance regimes may have directly and indirectly contributed to differences in habitat structure (Byrne, 2007) between the gardens and vacant lots.

36

The effect of habitat structure on belowground biocontrol activity differed with the type of biocontrol agent. Biocontrol activity of ants was significantly higher in vacant lots than in the gardens. The higher ant activity in vacant lots may be due to the greater habitat complexity both in the volume and numbers of distinct leaves of grassy and weedy species and less frequent disturbance compared to that in urban gardens. Being generalist predators with the ability to store food, ants are buffered against significant variations in prey density but are affected by abiotic factors like cultural practices followed in agroecosystems (Risch and Carroll, 1982; Symondson et al., 2002). Frequent irrigation leading to higher soil moisture and cool soil temperatures may limit harvesting of resources by ants (Kaspari et al., 2000). Other studies have also found habitat structure components including leaf litter, tree density, soil moisture, canopy cover, and complexity to influence ant diversity and composition (Clarke et al., 2008; Gotelli and

Ellison, 2002; Lassau and Hochuli, 2004; Sanford et al., 2009).

Microbial pathogens exhibited higher activity in urban gardens compared to vacant lots. A plausible explanation could be the potential domination of ant predation in vacant lots. Ant activity was higher in vacant lots which may have resulted in underrepresentation of biocontrol services provided by the microbes. Using two types of cages with different mesh sizes to allow or exclude larger ants, we demonstrated that biocontrol activity of ants differed significantly with activity being lower in cages with smaller mesh sizes as expected. However, activity of microbial pathogens did not differ significantly between the two cage-types, suggesting that ant predation can be ruled out as a factor for lower levels of biocontrol provided by microbes in vacant lots. A more pertinent explanation for higher biocontrol activity of microbial insect pathogens in

37 gardens as compared to vacant lots could be the higher plant diversity (Chapman and

Newman, 2010) and greater disturbance associated with cultural practices carried out in urban gardens. Cultural practices are known to have significant impact on microbial communities in soil with practices such as irrigation, no till, , residue addition and organic fertilizers favoring the growth of microbial populations (García-

Orenes et al., 2010; Kang et al., 2005; Nakhro and Dkhar, 2010). Indeed, there was higher soil moisture in urban gardens than in vacant lots in the same two cities in 2009 most likely due to the frequent irrigation of the gardens (Grewal et al., 2011). Also

Smitley and Rothwell (2003) found higher incidence of the bacterial pathogen

Pennibacillus sp. infection of black turfgass ataenius larvae in golf course rough (47.4%) compared with fairway (26.4%) which was more heavily managed. Thus, cultural practices and plant community composition, both of which influence habitat structure, may affect the composition and activity of microbial pathogens in the soil.

Entomopathogenic nematodes showed low activity in both vacant lots and urban gardens. Various abiotic and biotic factors may have contributed to this observed low activity. Limited activity of entomopathogenic nematodes in vacant lots is likely due to low potential host insect density, low soil moisture and high soil compaction whereas low activity in urban gardens is likely due to various cultural practices such as tillage, crop removal, and fertilizer applications (Barbercheck and Hoy, 2005; Koppenhofer and

Grewal, 2005). Alumai et al. (2006) recovered entomopathogenic nematodes from 43% of the golf course fairways and 57% of the rough areas, but none from the greens. They concluded that entomopathogenic nematodes are more likely to occur in less intensively managed sites that receive fewer chemical inputs and have relatively high sand, and

38 moderate silt, organic matter, phosphorus, and magnesium content. Nevertheless, the existence of naturally occurring entomopathogenic nematodes in urban soils suggests that the conditions suitable for their persistence do exist in urban ecosystems.

Differential effects of habitat structure on different groups of belowground organisms suggest that specific cultural practices need to be identified to enhance biocontrol services of specific groups of organisms. In this regard, further studies are needed to develop cultural practices that can enhance activities of beneficial bacterial and fungal communities and predatory species such as ants, beetles, spiders, and nematodes in urban landscapes. A thorough understanding of the influence of specific cultural practices which can be used as tools to manipulate specific components of habitat structure would enable the development of ecological approaches to increase ecosystem services of soil organisms in urban and agroecosystems.

2.6 Conclusions

This study finds a high level of potential naturally occurring biocontrol service in urban landscapes (51 to 98% mortality of baited insects) suggesting that the use of chemical pest control measures can be minimized if natural biocontrol services provided by the soil food web can be harnessed for the management of insect pests affecting urban agriculture. Higher biocontrol services provided by ants in vacant lots as compared to urban gardens supported the hypothesis that reduced habitat heterogeneity, increased moisture, and greater disturbance reduces natural biocontrol services rendered by ant communities. Ants were the major contributors of biocontrol activity followed by microbial communities in vacant lots, whereas in urban gardens, ants and microbial

39 communities contributed equally to the overall biocontrol service. Microbial pathogens had higher activity in urban gardens as compared to vacant lots. Both vacant lots and urban gardens exhibited low entomopathogenic nematode activity. Overall, this study provides the first baseline information on belowground biocontrol services provided by the soil food web in urban ecosystems which can serve as a foundation for the development of ecologically-based sustainable pest management practices and help guide further decision making regarding the use of vacant lots and pest management issues in urban landscapes. The manner by which the vacant lots are converted to urban gardens may benefit from considerations of the residing organisms and the significant beneficial ecological services they provide. Finally, this study contributes useful information on the ecology of vacant lots, an emerging issue in post-industrial cities in .

40

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Table 2.1. Site locations and their Physicochemical Soil Characteristics

SOIL % CITY/YEAR HABITAT ADDRESS pH TEXTURE SOM Akron/2009 Gardens Clay = 9-18% Vernon Odom Blvd. & Fern St. 7.13 2.99 Sand = 39-68% Cuyahoga St. & Uhler Ave. 6.81 4.47 Silt = 24-43% Charles St. & Turner St. 6.36 7.43 Newton St. & Iroquois Ave. - - Kenmore Blvd. & Ira Ave. 7.03 3.92 Inman St. & Morgan Ave 7.04 4.15 Vacant Lots Clay = 9-23% 1131 Arnold Ave. - - Sand = 34-72% 443 S Arlington St. 6.51 4.28 Silt = 19-43% 733 Moon St. 6.47 4.58 847 Garfield St. 6.88 3.64 107 W Tallmadge Ave. 6.19 4.38 297 Ira Ave. 6.64 5.74 Cleveland/2009 Gardens Clay = 6-20% W 14th & Mentor Ave 7.09 5.06 Sand = 28-60% St Claire Ave NE & E 23rd St. - - Silt = 28-66% Miles Ave & E 120th St. 7.29 4.92 3164 W 82nd St. 6.54 6.42 6205 Pear Ave. 5.99 24.55 W 574 Ithaca St. - - Franklin Blvd & W 38th St. 6.54 7.29 Vacant Lots Clay = 6-30% 7906 Vineyard Ave. 6.20 5.35 Sand = 27-87% 7008 Cedar Ave. 6.65 3.95 Silt = 19-47% 1971 W 57th St. - - 3703 Clinton Ave. 6.94 4.34 6017 Pear Ave 5.99 5.31 3614 E 82nd Ave. - - W 14th St. near Mentor Ave 7.33 4.29 Cleveland/2010 Gardens Clay = 6-20% 900 E. 72nd St./Blue pike 7.50 5.62 Sand = 28-60% 1227 Ansel Rd./Clear lake 5.61 4.48 Silt = 28-66% 2615 Lakeside Ave. E - - E. 46th & Quincy Ave. 7.58 15.36 E. 114th & Woodland Ave. 7.91 6.66 E. 79th St. & Amos Ave. 7.56 13.55 E. 54th St. & Fleet Ave. 7.59 10.38 2922 W 25th St. 7.54 11.91 1945 E. 66th St. 7.46 12.36 Vacant Lots Clay = 6-30% 7111 Linwood Ave 7.58 7.78 Sand = 27-87% 7320 Linwood Ave 7.70 7.12 Silt = 19-47% 7206 Lawnview Ave 7.78 8.07 1273 E 74th St. 7.37 6.21 1406 E 89th St. 7.90 6.34 1798 E 87th St. 7.96 6.29 th 1763 E 87 St. 7.71 6.31 10307 Churchill Ave. 7.54 7.93 8019 Pulaski Ave. 7.75 3.33 7920 Pulaski Ave. 7.78 5.76

SOM = Soil organic matter; - = data not available 46

Figure 2.1. Percentage mortality of Galleria mellonella in urban gardens (UG) and vacant lots (VL) in Akron (2009) and Cleveland (2009 and 2010). Different letters on the bars indicate significant differences at p<0.05.

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Figure 2.2. Percentage mortality of Galleria mellonella caused by different naturally occurring biocontrol agents in urban gardens and vacant lots over the two year study period in Akron and Cleveland. Different letters on the bars indicate significant differences at p<0.05.

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Figure 2.3. Percentage mortality of Galleria mellonella in urban gardens and vacant lots in Akron and Cleveland assessed by bait insects enclosed in cages with large (Cage 1) and small (Cage 2) mesh sizes. Different letters on bars indicate significant differences at p<0.05.

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Figure 2.4. Percentage mortality of Galleria mellonella caused by different naturally occurring biocontrol agents in urban gardens and vacant lots assessed by bait insects enclosed in cages with large (Cage 1) and small (Cage 2) mesh sizes. Different letters on bars indicate significant differences at p<0.05.

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CHAPTER 3: FACTORS AFFECTING BELOWGROUND BIOCONTROL ACTIVITY

IN URBAN LANDSCAPES

3.1 Abstract

Potential below ground biological control within urban gardens and vacant lots can achieve up to a 60% reduction in pest abundance with major contributions by ants, bacterial and fungal communities and entomopathogenic nematodes. However, these below ground biological control agents sensitive to variations in management practices used in urban gardens. In order to generate hypotheses regarding practices that could enhance below ground natural biocontrol activity, we determined the factors affecting belowground activity by quantifying existing below ground biocontrol activity using an in-situ insect baiting technique and soil quality/health parameters including a comprehensive nematode community analysis and soil physical and chemical analysis at the potential and existing urban garden sites in three Ohio cities: Cleveland, Columbus and Akron. We hypothesized that belowground biocontrol activity will positively correlate with the health of the soil food web and soil quality. We found that potential biocontrol service by ants(as assessed by mortality of bait insect caused by ants) is associated negatively with enrichment index and NH4-N; and positively with number of omnivore nematodes and soil moisture. In contrast, mortality by microbes is positively

51 associated with enrichment index, NH4-N, and negatively with the number of omnivore nematodes and soil moisture. Mortality by EPNs is associated positively with plant parasitic index, number of cp-1 class bacterial feeding nematodes, and negatively with combined maturity index, cp-2 class bacterial feeding nematodes and NO3-N.We also found significant differences in nematode community counts and indices and soil parameters between the cities but not between urban gardens and vacant lots. On the basis of our results we put forward intermediate disturbance hypothesis framework to design cultural practices that would enhance activity of belowground biocontrol agents in urban landscapes. We hypothesize that below ground biological control activity by microbes and ants will be higher in low intensity tillage, composted manure mulch (C:N

= 20) application, use and low intensity irrigation regime management conditions. The understanding of the dynamics of various below ground biological control agents under these proposed conditions can provide critical information to design cultural practices that can further enhance natural biocontrol services, minimizing the need for synthetic chemical or innundative biological pest control applications.

3.2 Introduction

Biological control is a potential alternative to chemical pest control and is compatible with most integrated pest management (IPM) measures. One of the forms of biological control is conservation biological control where the goal is to enhance natural enemy efficacy through modification of the environment or of existing pesticide practices

(Eilenberg et al., 2001). However, the environment in which these natural enemies work is complex, and a major problem is variable biocontrol activity due to variable biotic and

52 abiotic factors. Hence assessment of factors affecting biocontrol agents and their activity can provide valuable information on devising cultural practices to conserve them.

The activity of belowground natural enemies is often affected by disturbances.

Urbanization processes involve disturbances such as… and over time these land use changes can arthropod communities (McIntyre, 2000). In the early successional period, generalists predators predominate and over time specialist herbivore species establish depending on resource availability (Odum 1969; Brown 1985, Vincent and Frankie 1985;

Denys and Schmidt 1998). Urbanization may have both direct and indirect effects on soil organisms through habitat loss, habitat structure changes and resource availability

(McIntyre, 2000). Some species prefer sites under continuous disturbance like frequent mowing whereas some prefer intermediate level of disturbance (McIntyre, 2000).

We measured the impacts of disturbance on below ground biocontrol agents including ants, microbes and entomopathogenic nematodes which prey upon soil- dwelling stages of major insect pests in urban landscapes. Changes in ant community structure following disturbance has been well documented (Andersen, 1997b; Burbidge et al., 1992; Vasconcelos, 2008). Ant communities have also been studied in various urban landscapes (Sanford et al., 2008; Clarke et al., 2008; Lassau and Hochuli, 2004). Ants nest in the ground and forage on the soil surface.. Both richness and abundance of ant communities are vulnerable to the urban development, fertilization, farming practices and occurrence of human/animal/vehicle traffic in urban landscapes (Sanford et al., 2008;

Folgarait, 1998). Among the habitat structure, the key factors influencing ant communities include fragment size, edge effect, woody debris, tree density, soil moisture, canopy cover, and habitat complexity are all associated with decreases in ant diversity

53 and composition (Sanford et al., 2008; Clarke et al., 2008; Gotelli and Ellison, 2002;

Lassau and Hochuli, 2004). Being generalist predators with the ability to store food, ants are buffered from significant variations due to variations in prey density but are affected by abiotic factors like various cultural practices followed in agroecosystems (Symondson et al., 2001; Risch and Carroll, 1982). This suggests that they can be managed to enhance their abundance and distribution.

Few studies have addressed the effect of land use change on microbial activity. In general, microbial activity tends to decline several years after establishment of agriculture

(Diquelou et al., 1999and is reduced in new versus established residential landscapes

(references). To date, few have examined these agents in terms of the biocontrol services they provide. Given the importance of microbial activity to the suppression of pests below ground, it is critical to explore ecologically-based cultural practices for use in urban, agricultural, and natural ecosystems that could retain and enhance these organisms. Cultural practices may have significant impact on microbial communities in soil with practices such as irrigation, no till, crop rotation, residue addition and organic fertilizers favoring the growth of microbial populations (García-Orenes et al., 2010; Kang et al., 2005; Khonje et al., 1989; Nakhro, 2010). Such practices affecting the microbial communities in the soil need to be sought to enhance their activity and biocontrol services they provide.

Many abiotic and biotic factors affect EPNs including temperature, moisture, relative humidity, ultraviolet light, soil texture, and competition between different nematode species, competition with other insect pathogens, nematophagous fungi, collembolans, , tardigrades and predatory nematodes (Koppenhöfer, 2000). High

54 temperatures in the range of 30-40°C can inactivate IJs by increasing metabolism and depleting energy stores, while low temperatures in the range of 10-15°C lead to torpor

(Griffin, 1993; Grewal et al., 1994b). Low soil moisture and high soil compaction can also limit activity of EPNs (Baur and Kaya, 2002). Various cultural practices like tillage, crop removal, fertilizer and chemical pesticide applications are also associated with restricted EPN activity (Millar and Barbercheck, 2002; Grewal et al., 1998; Patel and

Wright, 1996). A recent study by Alumai et al. (2006) suggested that EPNs are more likely to occur in less intensively managed turfgrass sites that receive fewer chemical inputs and have relatively high sand, and moderate silt, organic matter, phosphorus, and magnesium content. More such studies are needed for the development of conservation approaches for the use of EPNs, particularly in urban landscapes.

In this study we aim to assess potential and existing urban garden sites for soil quality/health, existing below ground biocontrol activity to identify factors that influence and enhance below ground natural biocontrol activity. We hypothesize that belowground biocontrol activity will positively correlate with the health of the soil food web and soil quality. Due to differences in habitat structure and disturbance regime, we also expected to see differences in soil quality/health parameters between urban gardens and vacant lots as well as in between different cities.

3.3 Methods

3.3.1 Study sites

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Twenty six urban gardens and thirty four vacant lots were studied for soil characteristics and belowground biocontrol services provided by soil invertebrates and microorganisms during the summer of 2009, 2010, and 2011 in three Ohio cities:

Cleveland, Akron and Columbus. The cities have average monthly temperatures in the range of 26.4°F – 28°F in January and 71.3°F - 75°F in July and average annual precipitation of 91.9 to 101.3 cm. The community gardens in Akron were established in

2009 (i.e. were 3-4 months old when the study was undertaken), those in Columbus were established between 2003-2008 and those in Cleveland were much older (the majority being 15-30 years old).

The commonly planted species of vegetables and fruits in the community gardens were: Solanum lycopersicum (tomato), Solanum tuberosum (potato), Daucus carota

(carrot), Cucurbita pepo (zucchini), Cucurbita mixta (pumpkin), Lactuca sativa var. longifolia (romaine lettuce), Capsicum annuum (bell pepper), Cucurbita moschata

(squash), Phaseolus vulgaris (beans), Brassica oleracea (cabbage), Brassica oleracea

(broccoli), Rubus idaeus (raspberry), Vitis vinifera (grape), Spinacia oleracea (spinach),

Pisum sativum (pea), Brassica oleracea var. acephala (cole), Citrullus lanatus

(watermelon), Cucumis melo (cantaloupe), Mentha sachalinensis (mint), Brassica oleracea (cauliflower), Prunus avium (cherry), Raphanus sativus (radish), Zea mays

(maize), Allium sativum (garlic), Helianthus annuus (sunflower), Solanum melongena

(eggplant), and Ipomoea batatas (sweet potato). The gardens were also regularly tilled, weeded, and irrigated but had no pesticide inputs except for occasional fertilizer applications.

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In contrast, the vacant lots were typically covered in grassy and weedy species and were occasionally mowed to look like urban lawns. The majority were predominantly covered in turfgrass and associated weedy species such as Poa annua (annual bluegrass),

Digitaria ischaemum (smooth crabgrass), Festuca arundinacea (tall fescue), and

Taraxacum officinale (dandelion), Trifolium pratence (trophy clover), Rhus typhina

(staghorn sumac), (purple loosestrife), Lonicera spp (bush honeysuckle), Sambucus canadensis (american elder), Rumex obtusifolia (broadleaf dock), Cichorium intybus (chicory), Phalaris arundinacea (canarygrass), Elytrigia repens

(quachgrass) and Acer negcindo (boxelder).

3.3.2 Quantification of belowground biocontrol activity and identification of potential biocontrol agents

Belowground insect biocontrol services were quantified in Cleveland, Akron and

Columbus plots using methods described in Chapter 2 with in-situ baiting technique and identification of the potential biocontrol organisms according to signs shown by the bait insect cadaver. In Cleveland and Akron, each plot was divided into 3-4 sub-sites as described in Chapter 2 whereas in Columbus, each plot was divided into two sub sites representing house footprint and backyard. On each sub site, 6 locations were chosen on a linear transect to bury the cages containing 3-5 Galleria mellonella larvae as baits per cage. All the cages were recovered after two days and the G. mellonella larvae were sorted as dead or alive and all living larvae were observed for two additional days to record any additional mortality and signs of pathogen infection. The death of each G.

57 mellonella larva was attributed to a pathogen or predator based on physical condition, color, hardness and smell of the cadaver (Tanada and Kaya, 1993) as described in

Chapter 2.

3.3.3 Soil sample collection

Soil samples were collected from all the sites using a 2-cm diameter soil probe.

Each site was divided into two (for Columbus sites), three (for Akron sites) or four (for

Cleveland sites) approximately equal sections. To account for the aggregated spatial distribution of nematodes (Barker et al., 1969) in soil, 9 soil cores, 10 cm deep, were taken from each section and combined to form a composite sample per section. Soil samples were placed in polyethylene bags and stored at 4°C before analysis to minimize changes in nematode populations and biochemical reactions (Barker et al., 1969).

3.3.4 Soil nematode extraction and identification

The Baermann funnel technique was used to extract nematodes from soil samples

(Flegg and Hooper 1970). Composite samples were mixed well and 20 gm soil from each of these composite samples was placed on a Baermann funnel. After 72 h, nematodes in the water were collected in plastic vials through a rubber tube attached beneath each funnel. After allowing the nematodes to settle overnight at 4°C, the upper layer of water was carefully discarded without disturbing the settled nematodes. The nematodes were then killed at approximately 50°C by adding an equal amount of boiling water. Finally, using an inverted microscope and gridded petri dish, the nematodes were counted and identified to genus level using morphological characteristics and published keys (Goodey

58

1963; Mai and Lyon 1975). All identified nematode genera were assigned to one of the five tropic groups according to Yeates et al. (1993): Bacterivores (BF), Fungivores (FF),

Plant parasites (PP), Predators (PR), and Omnivores (OM). Nematode genera were also classified along a colonizer-persister (c-p) continuum of 1 to 5 according to Bongers

(1990). Nematodes with a c–p value of 1 are short lived, have high fecundity, and feed on enriched media whereas those of a c–p value of 5 have a long life span, low fecundity, and are predominantly omnivores and predators (Bongers 1990).

3.3.5 Nematode community index calculation

Maturity index was calculated as the weighted mean of the individual cp classes:

MI = Σ v(i)· f(i), where v(i) is the cp value of taxon i and f(i) is the proportion of that taxon in a nematode community (Bongers, 1990). In the study, four different variations of

MI were calculated: free-living nematodes with cp-1 though cp-5 (MI), plant-feeding nematode with cp-2 through cp-5 (PPI) and combined free-living and plant-feeding nematodes with cp-1 through cp-5 (Combined MI) (Bongers, 1990; Bongers and

Korthals, 1994; Yeates, 1994).

Enrichment index (EI) and structure index (SI) were calculated according to

Ferris et al. (2001). EI and SI use a weighting system based upon the importance of the functional guilds along hypothesized trajectories of enrichment and structure of soil nematode foodweb and are calculated as: EI = 100 · [e / (e + b)], SI = 100 · [s / (s + b)], where b = Σkb·nb e = Σke·ne, and s = Σks·ns. Basal components (b) of the food web

(fungal and bacterial feeders in the c-p 2 guild) were calculated as b = Σkbnb where kb is the weighted constant for the guild, and n is the number of nematodes in that guild.

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Enrichment (e) and structure (s) components will be similarly calculated, using nematode guilds indicative of enrichment (bacterivores of c-p 1, and fungivores of c-p 2), and guilds supporting structure (bacterivores of c-p 3-5, fungivores of c-p 3-5, omnivores of c-p 3-5, and predatory nematodes of c-p = 2-5).

3.3.6 Soil physical and chemical parameters

Soil pH was determined using a pH electrode by mixing with de-ionized water in a 1:1 ratio. To measure soil organic matter, the weight loss during ignition was calculated by using approximately 10 g of fresh soil in a pre-weighed glass vial and drying the samples at 360°C (Storer 1984). Nutrients such as P, K, Ca, and Mg, as well as percent carbon and nitrogen by soil dry weight were analyzed using the Mehlich 3 extraction,

ICP analysis, Dumas method and elementary analysis by the STAR lab at the Ohio

Agricultural Research and Development Center (Mehlich 1984; Sommers and Nelson

1972; AOAC 1989; ISO 1995).

3.3.7 Data analyses

All G. mellonella larval responses were measured as binary variables. Proportion of larvae killed in each section of each site was recorded as percentage (%) larval mortality by pooling data from all the six locations on each transect in that section. The percentage mortality data were used as an index of biocontrol activity. Nematode population data were transformed to ln (x+1) and mortality data were arcsine transformed prior to statistical analysis to normalize the variance. Different cities as well as urban garden and vacant lot sites were compared for nematode trophic groups, various food web indices,

60 and soil properties, using general linear mixed model ANOVA. Scatter plot plotting EI and SI was used to provide a model framework of nematode faunal analysis as an indicator of the likely conditions of the soil food web (Ferris et al. 2001).. The software package used was MINITAB v.15 (Minitab, Inc, State College, PA). A P value ≤ 0.05 was considered significant. We used canonical correspondence analysis to correlate the mortality data (indicating potential biocontrol activity) including total mortality as well as mortality caused by specific agents with soil quality/health variables including various biotic and abiotic variables using XLSTAT program in excel.

3.4 Results

3.4.1 Biological control in urban gardens and vacant lots of three Ohio cities: Cleveland,

Akron and Columbus

Similar to the results in Chapter 2, mean total mortality in both urban gardens and vacant lots in the three Ohio cities as assessed by % mortality ranged between 63% and

82%. Total mortality did not differ between urban gardens and vacant lots however mortality due to ants and microbes varied between gardens and lots. Mortality by ants was significantly higher in vacant lots than in urban gardens (p = 0.04) whereas mortality by microbes was significantly higher in urban gardens than in vacant lots (p = 0.002)

(Figure 3.1).

3.4.2 Nematode community characteristics of urban gardens and vacant lots

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The nematode community faunal analysis reflects disturbances through movement of values from one quadrant to another, signifying a range from stressed and disturbed to enriched and stable. The scatter plots for the food web faunal profile (with the

Enrichment Index on the y-axis and the Structure Index on the x-axis) for Akron,

Cleveland, and Columbus indicate that both urban garden as well as vacant lot sites

(Figure 3.2) were highly enriched and poorly to moderately structured (quadrant 1).

Akron sites in general followed this trend, whereas some Cleveland and Columbus sites were more structured and matured.

The ANOVA results for nematode community analysis are summarized in Table

3.1. Total number of nematodes, FLN, and PPNs were lower in general in Columbus sites as compared to Cleveland and Akron sites (Figure 3.3). Though there was a trend of higher number of nematodes in vacant lot sites in all cities as compared to the urban garden sites, the trend was not significant (Figure 3.3) except for PPNs which were higher for Akron and Columbus vacant lots. Among the FLN group, only fungivores were in significantly higher numbers in Akron (Figure 3.4). Akron sites showed significantly higher diversity with higher number of genera than Cleveland sites (p =

0.003) (Figure 3.3). Akron sites also exceeded significantly in the number of PPNs compared to the Cleveland (p = 0.022) and Columbus sites (p = 0.03) and in combined

Maturity Index (MI) compared to the Cleveland sites (p = 0.002); but had lower

Enrichment Index (EI) compared to the Cleveland (p = 0.035) and Columbus sites (p value= 0.03) (Figure 3.3 and 3.5). Columbus sites on the other hand exceeded significantly in Structural Index (SI) as compared to the Cleveland sites (p = 0.002)

(Figure 3.5). Though we found significant differences in nematode abundances and

62 community indices among different cities in general, after accounting for the city differences and variability in between urban gardens or vacant lots, we did not find any significant differences between garden and vacant lot sites (Table 3.1). However, nematode counts/indices showed large variation between similar plot categories (gardens or vacant lots) and failure to find any difference between gardens and vacant lots could be attributed to this large variability.

3.4.3 Soil chemical characteristics in urban gardens and vacant lots

The ANOVA results for soil chemical analysis are summarized in Table 3.2.

Mean soil pH in Akron garden and vacant lot sites was 6.87±0.34 and 6.54±0.29 respectively; in Cleveland 7.158±0.693 and 7.41±0.59; and in Columbus 7.56±0.11 and

7.5±0.11 respectively. Soil pH in Akron plots (both gardens and vacant lots) was significantly lower than Cleveland (p = 0.026) and Columbus plots (p = 0.005) (Figure

3.5). Akron plots also had significantly lower carbon than Cleveland (p = 0.022) and

Columbus plots (p = 0.016). After accounting for the city differences and variability between similar category plots (urban gardens or vacant lots), soil carbon in general was found to be lower in vacant lots than garden sites with this trend being more prominent for Cleveland plots (p = 0.008) (Figure 3.6). Phosphorus, magnesium and cation exchange capacity (CEC) were also found to be significantly higher in garden sites (p value <0.001 for P and Mg and 0.009 for CEC) compared to vacant lots but trend was more obvious for Cleveland plots (Figure 3.6).

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3.4.4 Nematode community characteristics and abiotic soil parameters affecting potential biological control activity

The ordination diagram (Figure 3.7) shows relationship between mortality by different biocontrol agents and soil quality/health parameters. The figure shows two canonical axes in horizontal and vertical directions and arrows represent different soil quality/health parameters. Correlations between different variables and between variables and canonical axes are depicted by direction of the arrows whereas the length of the arrows represents the relative contribution of the variables to the axes. The eigenvector analysis (Figure 3.8) shows that most of the inertia is carried by the first axis (70.89%) and with the second axis we obtain 96.8% of the inertia. This suggests that the two- dimensional Canonical correspondence analysis map will be sufficient to analyze the relationships between the mortality contribution by specific agents and soil health/quality parameters.

The first axis is most closely aligned with the Enrichment index, Maturity index, number of bacteria feeding nematodes of cp-2 class, number of genera of nematodes, and soil moisture; whereas the second is most closely aligned with the combined maturity index, plant parasitic index, number of bacteria feeding nematodes of cp-1 class, and combined MI (Figure 3.8 and Table 3.3). Other biotic and abiotic variables contribute almost equally to both the axes. The ordination diagram also depicts specific variables correlating with total mortality of bait insect and mortality by specific agents. Potential ant biocontrol activity (as assessed by mortality of bait insects by ants) is associated negatively with enrichment index and NH4-N; and positively with number of omnivore nematodes and soil moisture. In contrast, mortality by microbes is positively associated

64 with enrichment index, NH4-N, and negatively with the number of omnivore nematodes and soil moisture. Mortality by EPNs is associated positively with plant parasitic index, number of cp-1 class bacterial feeding nematodes, and negatively with combined maturity index, cp-2 class bacterial feeding nematodes and NO3-N. The permutation test, testing null hypothesis that the mortality data (potential biocontrol activity) are not linearly related to the soil health/quality variables variables, was not significant (p value=0.062). However, as the p-value is just above the threshold we had chosen (0.05 against 0.062), the conclusion might not be as obvious. Furthermore, we are interested in checking if this is true for all variables, or if some variables seem to explain the results better than other.

3.5 Discussion

The performance of natural enemies in agricultural systems can significantly affect the population dynamics of the prey and hence enhancing predator response is an effective pest control strategy. In this three year study of urban gardens and vacant lots in three Ohio cities, we examined biocontrol services provided by soil foodweb, soil health and soil quality parameters. We found significant differences in soil nematode abundances and community indices between the cities but not between urban gardens and vacant lots. This could be due to large variability in these parameters between different urban gardens as well as vacant lots. Soil carbon, Phosphorus, magnesium and cation exchange capacity (CEC) were found to be significantly higher in garden sites compared to vacant lots. We also found that biocontrol services are affected by various nematode community variables and soil quality parameters like nematode maturity index, structural

65 index, enrichment index, total number of free living nematodes, soil moisture, pH, soil organic matter and some soil minerals like P, K and Ca.

Most of the sites in all three cities fell in quadrant 1 in nematode faunal profile analysis indicating highly enriched and low to moderately structured food webs. Hence, enrichment opportunistic nematodes of low c–p values dominated most of the sites. This suggests that these soil food webs are dominated by bacteria-driven decomposition pathways indicating a disturbed food web. This is in contrast to highly structured and poor to moderately enriched food webs of undisturbed natural grasslands and forest systems (de Goede and Bongers 1998; Ferris et al. 2001). Most of the Akron urban garden plots in general were less structured than Columbus and Cleveland plots. This could be attributed to the recent physical disturbance associated with garden establishment in Akron sites which were established only 3-4 months prior to the study was undertaken. Such disturbance could be detrimental to more sensitive groups of nematodes, especially those with high c–p values (Briar et al. 2007; Park et al. 2010).

Opportunists like bacterivores and plant parasitic nematodes (typical low c-p value nematodes) are often the first to recover, and omnivores and predators (high c-p value groups) are often among the last to recover (Bongers & Bongers, 1998; Ferris et al.,

2001) accounting for low SI in Akron gardens. High number of plant parasitic nematodes, opportunistic group, in Akron gardens suggesting that these are highly disturbed sites where high c-p value nematodes have not established well further supports this notion. In contrast, Columbus and Cleveland urban garden sites were older and likely recovered from the original disturbance of garden establishment.

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Total number of nematodes and FLN (fungivores in particular) were lower in general in Columbus sites as compared to Cleveland and Akron sites suggesting that urban ecosystem in Columbus has low (Ritz and Trudgill 1999). The productivity of urban ecosystems depends on soil parameters and proportion of area settled by plants indicating biomass of the site (Rebele, 1994). Majority of Columbus sites were vacant lots low in plant cover likely leading to low productivity. A severe long-term disturbance from heavy metal build-up such as arsenate in Columbus sites

(Sharma et al., unpublished data) may also have led to reductions in these nematode groups (Georgieva et al., 2002).

Some soil parameters varied between different cities and between garden and vacant lot sites in general. Akron sites had lower soil pH and soil carbon than Cleveland and Columbus sites. Soil carbon, phosphorus, and magnesium were in general higher in garden sites most likely due to frequent organic amendments like compost and use of fertilizers in these sites. In addition, CEC was also higher in garden sites (again).

Compost increases organic material, including humus, and by doing so it raises CEC of soil making nutrients less likely to leach away and stabilizing soil pH (Que`draogo et al.,

2001; Leifeld et al., 2002).

Canonical correspondence analysis to assess the relationship of various variables on total potential biocontrol as well as biocontrol by individual agents suggested that both biotic and abiotic factors play an important role. Ant activity was found to be associated negatively with enrichment index and NH4-N; and positively with number of omnivore nematodes and soil moisture.. Our result on the association between ants and soil moisture is similar to Wang et al. (2001). Ant activity increases along the moisture

67 gradient (Kaspari, 2000; Sanders et al., 2003; Whitford et al., 1999). Ants, being thermophilic, are sensitive to increasing moisture, increasing shade, and increased nitrogen (which can increase both soil moisture and shade) (Dahms et al., 2005).

Consistent with this, we found that EI, and NH4-N are negatively associated with ant activity suggesting that heavy nutrient enrichment and increased nitrogen seem to inhibit ant activity. In addition, ant activity was positively associated with number of omnivore nematodes suggesting that ants prefer less disturbed sites. Hence, high intensity management by cultural practices like tillage will affect ant activity negatively. Ants may be affected transiently by cultivation practices (sowing and harvesting) due to disruption to the habitat and nesting places of ants (Lobry de Bruyn, 1993). However, when coupled with high intensity management, such effects could be long lasting. Mitchell et al. (2002) observed higher ant abundance and richness in small forest patches with histories of more intense land use rather than large patches with minimal past land use.

In contrast to ant biocontrol activity, microbial biocontrol activity was positively associated with enrichment index, NH4-N, and negatively with the number of omnivore nematodes and soil moisture. Hence enriched less stable conditions support microbial biocontrol activity suggesting that cultural practices like residue addition and organic fertilizers will favor microbial activity as suggested by previous studies (Khonje et al.,

1989; Nakhro, 2010). Analysis showed that negative association of potential microbial bioontrol activity with soil moisture. Though moisture enhances microbial activity (Qiu et al., 2005; Kaspari , 2000), intensive irrigation regime can saturate the soil leading to decreased porosity, and decreased microbial activity (Dahms et al., 2005; Chapin, 2002).

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EPN activity was associated positively with plant parasitic index and number of cp-1 bacterial feeding nematodes, and negatively with combined maturity index, cp-2 class bacterial feeding nematodes and NO3-N. Both increase in plant parasitic index and number of cp-1 bacterial feeding nematodes indicates enriched nutrient condition of soil leading to increased growth of plants and enrichment opportunists (Bongers et al., 1997).

This is consistent with the findings from previous studies (Bednarek and Gaugler, 1997;

Shapiro et al., 1996) who found that NPK fertilizer suppressed applied nematode densities and whereas organic manure (indicating enrichment of soil) helped in establishing EPNs. Negative association with cp-2 class bacterivores, which are general opportunists thriving in disturbed environments, suggests that EPN activity is low in sites subjected to frequent disturbance. Consistent with this finding, we saw low activity of

EPNs (0-10% mortality of bait insect) in both urban gardens and vacant lots most likely due to associated disturbance of cultural practices like tillage, crop removal, fertilizer and chemical pesticide applications in urban gardens and frequent mowing of vacant lots.

Further investigation of these findings through intervention studies is needed to make recommendations on practices to be followed to enhance natural belowground biocontrol activity.

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Figure 3.1. Percentage mortality of Galleria mellonella caused by different naturally occurring biocontrol agents in urban gardens and vacant lots over three year study period in Akron, Cleveland and Columbus, Ohio. Different letters on the bars indicate significant differences at p<0.05.

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Figure 3.2. Nematode food web conditions in community gardens and vacant lots in Akron and Cleveland, Ohio, USA

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Figure 3.3. Total, free-living, and plant-parasitic nematode populations, and number of nematode genera in community gardens and vacant lots as well as in general in all the sites in Akron, Cleveland and Columbus, Ohio, USA. Data presented are Mean + SD. Different letter(s) on bars indicate significant difference (p<0.05).

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Figure 3.4. Components of free-living nematodes: Bacteriovores (Ba), Fungivores (FF), Omnivores (OM) and Predatory (PR) nematode populations in all the sites in Akron, Cleveland and Columbus, Ohio, USA. Data presented are Mean + SD. Different letter(s) on bars indicate significant difference (p<0.05).

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Figure 3.5. Nematode Structure Index, Enrichment Index, Maturity Index, Plant-parasitic Index, and Combined Maturity Index in community gardens and vacant lots as well as in general in all the sites in Akron, Cleveland and Columbus, Ohio, USA. Data presented are Mean + SD. Different letter(s) on bars indicate significant differences (p<0.05).

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Figure 3.6. Total soil carbon (% C), pH, Magnesium, Phosphorus, Potassium and Cation exchange capacity in community gardens and vacant lots in Columbus, Cleveland, ± Akron, Ohio, USA. Data presented are Mean +/± SD. Different letter(s) on bars indicate significant difference (p<0.05).

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Table 3.1. F- and p-values from GLM ANOVA mixed/nested model on nematode community and soil property analysis for samples collected comparing community gardens and vacant lots in three cities of Ohio: Akron, Cleveland, and Columbus ______

Parameter F-value P-value ______

Free-Living Nematode Population 0.02 0.882 Bacterivores 1.23 0.270 Fungivores 1.42 0.236 Omnivores 0.03 0.855 Predators 0.35 0.555 Plant-Parasitic Nematode Population 3.42 0.071 Nematode Genera 0.08 0.777 Maturity Index 0.03 0.872 Plant Parasitic Index 2.17 0.287 Combined Maturity Index 2.15 0.149 Enrichment Index 0.33 0.57 Structure Index 0.73 0.397 ______

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Table 3.2. F- and p-values from GLM ANOVA mixed model on soil mineral analysis for samples collected comparing community gardens and vacant lots in two cities of Ohio: Cleveland, and Columbus ______

Parameter F-value P-value ______pH 0.19 0.661 % C 7.58 0.008* P 20.46 <.0001* K 0.01 0.904 Ca 3.35 0.07 Mg 13.08 <.0001* CEC 7.21 0.009* % N 5.16 0.025* ______

% C - total soil carbon; Mg – Magnesium; P – Phosphorus; K – Potassium; CEC - Cation exchange capacity; Ca –Calcium; % N - total nitrogen.

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CCA Map / Objects (axes F1 and F2: 95.92 %) 1.2 MORTALITY BY EPNs BF1 0.8 PPI MI pH G SI PPN 0.4 MicBN MORTALITY BY ANTS NH4-N

0 OM MORTALITY BY TOTAL MORTALITY MICROBES EI -0.4 SOM NO3-N %C PR FF

F2 (26.83 %) (26.83F2 Moisture -0.8

-1.2 BF2

-1.6 Com MI

-2 -2.8 -2.4 -2 -1.6 -1.2 -0.8 -0.4 0 0.4 0.8 1.2 1.6 2 2.4 F1 (69.10 %)

Objects Variables

Figure 3.7 Canonical correspondence analysis of the relationship between mortality by different biocontrol agents and various biotic and abiotic soil quality/health variables in urban landscapes of three Ohio cities where the direction of arrows indicates correlation with the first two canonical axes and the length of arrows represents the strength of the correlations.

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Table 3.3. Regression coefficients giving the linear combination of standardized variables that compose the first two canonical axes in a canonical correspondence analysis of the relationship between mortality by different biocontrol agents and various biotic and abiotic soil quality/health variables in urban landscapes of three Ohio cities

Regression coefficients:

First Second canonical axis canonical axis

ln BF1 0.361 0.987 ln BF2 0.737 -1.160 Ln FF+1 -0.314 -0.566 Ln OM+1 -0.321 -0.154 Ln PR+1 0.010 -0.457 ln(G+1) -0.795 0.478 ln(PPN+1) 0.280 0.461 PPI -0.013 0.774 MI 1.175 0.783 Com MI -0.044 -1.646 EI 0.796 -0.229 SI -0.453 0.387 pH 0.386 0.538 Moisture -0.931 -0.639 NH4-N 0.246 0.091 NO3-N 0.108 -0.429 MicBN 0.131 0.194 SOM -0.339 -0.453 %C -0.339 -0.453

85

F1 F2 F3 Eigenvalue 0.124 0.048 0.007 Constrained inertia (%) 69.098 26.827 4.075 Cumulative % 69.098 95.925 100.000 Total inertia 25.334 9.836 1.494 Cumulative % (%) 25.334 35.170 36.664

Scree plot

0.14 100

0.12 80

0.1

60 0.08

0.06 Inertia (%) Inertia Eigenvalue 40

0.04 20 0.02

0 0 F1 F2 F3 axis

Figure 3.8 Eigen values and percentages of inertia of the first three canonical axes (F1,

F2 and F3) from canonical correspondence analysis presen]ted in the tabulated form and as a scree plot.

86

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