Habitat structure influences below ground biocontrol services: A comparison between urban gardens and vacant lots
Highlights
► Urban agriculture provides local self-reliance in post-industrial cities. ► Harnessing natural services of the soil food web is critical in urban agriculture. ► Soil food web can provide substantial biocontrol service in urban ecosystems. ► Ants provided higher natural biocontrol in urban vacant lots than gardens. ► Microbial pathogens provided higher biocontrol in gardens than vacant lots.
Introduction
Urban agriculture offers a comprehensive framework for local self-reliance and resilience and a means to reducing the ecological footprint of cities (Grewal & Grewal, 2011). Interest in urban agriculture has escalated recently due to the accumulation of vacant land particularly in post-industrial U.S. cities (Callis & Cavanaugh, 2009) 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 & 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, Puppim de Oliveira et al., 2011). An important regulatory ecosystem service associated with biodiversity is natural pest control (Gurr, Wratten, & Luna, 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 these studies have addressed species richness 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, Roze, & Francez (1999) found that microbial activity tends to decline several years after establishment of agriculture. Scharenbroch, Lloyd, and Johnson-Maynard (2005) found that old residential landscapes had higher microbial biomass than new residential landscapes most likely due to greater time since disturbance. Similarly, Park, Cheng, McSpadden Gardener, and Grewal (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, Gruner, & Kaplan, 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 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.
Section snippets
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 91.9–101.3 cm. We identified six community gardens and six nearby (within 1 mile)
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) (Fig. 1). When examined separately for each city
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, López and Potter, 2000, Potter, 2005). This two year study of urban gardens and vacant
Conclusions
This study finds a high level of naturally occurring biocontrol service in urban landscapes (51–98% 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,
Acknowledgements
This work was supported by The Ohio State University's Urban Landscape Ecology Program, the OARDC Research Internships Program, and the National Science Foundation's Urban Long Term Research Area Exploratory (ULTRA-EX) program. We thank city officials in Akron and Cleveland, urban community gardeners, and the staff at the Cleveland Botanical Garden for allowing us to use the vacant lots and community gardens for this study.
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