Habitat structure influences below ground biocontrol services: A comparison between urban gardens and vacant lots

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 organism. 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-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.

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.