The Value of Urban Vacant Land to Support Arthropod Biodiversity and Ecosystem Services Author(s): Mary M. Gardiner , Caitlin E. Burkman and Scott P. Prajzner Source: Environmental Entomology, 42(6):1123-1136. 2013. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/EN12275

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REVIEW: COMMUNITY & ECOSYSTEM ECOLOGY

The Value of Urban Vacant Land to Support Arthropod Biodiversity and Ecosystem Services MARY M. GARDINER,1 CAITLIN E. BURKMAN,

AND

SCOTT P. PRAJZNER

The Ohio State University, Ohio Agricultural Research and Development Center, 1680 Madison Avenue, Wooster, OH 44691

Environ. Entomol. 42(6): 1123Ð1136 (2013); DOI: http://dx.doi.org/10.1603/EN12275

ABSTRACT The expansion of urban areas is occurring globally, but not all city neighborhoods are gaining population. Because of economic decline and the recent foreclosure crisis, many U.S. cities are demolishing abandoned residential structures to create parcels of vacant land. In some cities, weak housing markets have, or will likely, recover in the near term, and these parcels will be redeveloped. However, in other cities, large numbers of abandoned parcels have no signiÞcant market value and no likelihood of near-term redevelopment. The creation of these vacated green spaces could offer opportunities to preserve declining species, restore ecosystem functions, and support diverse ecosystem services. Arthropods are an important indicator of the ability of urban vacant land to serve multiple functions, from conservation to food production. Across Europe, vacant lands have been found to support a diversity of rare species, and similar examinations of arthropods within this habitat are underway in the United States. In addition, using vacant land as a resource for local food production is growing rapidly worldwide. Arthropods play key roles in the sustainability of food production in cities, and land conversion to farming has been found to inßuence their community composition and function. A greater focus on quantifying the current ecological value of vacant land and further assessment of how changes in its ecosystem management affect biodiversity and ecosystem processes is clearly needed. Herein, we speciÞcally focus on the role of arthropods in addressing these priorities to advance our ecological understanding of the functional role of vacant land habitats in cities. KEY WORDS vacant land, brownÞeld, urban agriculture, natural enemy, pollinator

More than half of the worldÕs population is concentrated within cities (Liu et al. 2007, Pickett et al. 2011), and these ecosystems are inßuenced by the economic, social, and cultural conditions of the human communities living and working in them (Mcdonnell and Pickett 1990, Grove et al. 2002, Faeth et al. 2005). Although many parts of our world are experiencing rapid urban growth, economic decline and the recent foreclosure crisis have resulted in population decline within some U.S. cities (Silva 2010). These conditions have transformed the landscape of affected cities to include a signiÞcant number of vacant land patches (Keating 2010). In some cities, vacant land can be viewed as a temporary state, with a high likelihood for economic redevelopment (Pagano and Bowman 2000). However, when population growth is unlikely and vacant parcels have little to no real estate value, they are considered permanently vacated rather than temporally vacant. A city containing a signiÞcant quantity of these permanently vacated lands are sometimes referred to as “shrinking cities,” deÞned as an urban area that has experienced signiÞcant population loss, protracted economic downturn, or both (Reckien and MartinezÐFernandez 2011). Examples include CleveThis review is an invited article. 1 Corresponding author, e-mail: [email protected].

land, OH, and Detroit, MI. Cleveland currently contains 20,000 vacant parcels totaling 14 km2 (Cleveland Land Lab 2008; Fig. 1), and ⬇1,000 additional foreclosed structures are being demolished annually. Furthermore, Detroit has ⬎66,000 vacant lots totaling at least 103 km2, representing 28% of the cityÕs land area (Uno et al. 2010). The socioeconomic conditions within a city can often be correlated with the ecological conditions found within its ecosystems (Grove and Burch 1997, Grove et al. 2002, Pickett et al. 2011). Examples include watersheds in Baltimore, MD, where communities with higher levels of income and education are more likely to contain areas of green space compared with lower-income communities (Grove and Burch 1997). Similarly, Hope et al. (2003) reported an increase in plant diversity was correlated with family income and housing age within the Phoenix, AZ metropolitan area, and described this “luxury effect” as part of urban ecosystem functional structure. This inequitable allocation of green investment is a key concern of many stakeholders and can be addressed as cities develop conservation and management plans for vacant lands. Plant communities are often the only directly managed biota in urban environments and constitute the “template” on which animal populations are structured (Faeth et al. 2011). An examination of arthropod

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Fig. 1. In 2013, Cleveland, OH, contained ⬎3,500 acres of vacant land representing ⬎20,000 parcels. (Map courtesy of Terry Schwarz, Director, Cleveland Urban Design Collaborative, Kent State University.)

communities and their interactions can provide signiÞcant insight into how approaches to urban revitalization, a process largely deÞned by vegetation change and management, may impact ecosystem structure and function. Given their relatively short generation times, arthropod populations respond quickly to changes in the urban environment, making them key indicators of how land use change inßuences biodiversity (McIntyre 2000, McIntyre et al. 2001). In addition, the presence of these underutilized habitats within cities affords an opportunity to conserve and enhance the supporting, provisioning, regulating, and cultural ecosystem services within low-income neighborhoods. These include arthropod-mediated ecosystem services such as pollination, decomposition, nutrient cycling, and biological pest control (Isaacs et al. 2009). Mini-Review Article Scope In this article, we examine the ability of vacant lands to support threatened and endangered species, and beneÞcial arthropods that supply ecosystem services to urban landscapes. We draw from studies in the United Kingdom and continental Europe where researchers have long been interested in the ecology of urban brownÞelds (also referred to as derelict, postindustrial, wasteland, or ruderal habitats; Sukopp 2002). These include previously built sites but also landÞlls, industrial dumps, and abandoned railroad corridors (Strauss and Biedermann 2006). Herein, we refer to these habitats as vacant land and concentrate on stud-

ies examining previously built industrial or residential sites. As urban vacant land areas have expanded in U.S. cities, studies of arthropods and their functions have followed (Grewal et al. 2010, 2011; Uno et al. 2010; Yadav et al. 2012; Gardiner et al. 2013). We examine how knowledge gained from these and other studies of urban and suburban green spaces can aid in our understanding of urban ecosystem management. We also evaluate the importance of entomological research in greening initiatives and the conversion of vacant land to urban farms. Here, we examine the impacts and implications for arthropods and the functions and services they support within the changing urban landscape. Vacant Land Supports Arthropod Biodiversity Vacant land represents a substantial and growing habitat within several U.S. cities; thus, understanding their ecological value is important to the advancement of urban ecology and ecosystem management. Vacant lands are often ignored in conservation planning (Harrison and Davies 2002, Muratet et al. 2007, Kattwinkel et al. 2011), but several arthropod surveys in Europe have reported that these natural habitat analogues (Eversham et al. 1996) have the potential to be valuable reservoirs of biodiversity. For example, JacobÐ Remacle (1984) found 57 species of aculeate Hymenoptera using vacant lots as a foraging habitat within the city of Liege, Belgium. In the United Kingdom, Wright (1988) found 130 species of hover ßies (Syrphidae) including several rare or vulnerable species

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within many former industrial sites throughout the city of Coventry. Gibson (1998) reported that 12Ð15% of United Kingdom nationally scarce and rare species use urban vacant lands as a habitat; this range was considered an underestimate at the time because of limited inventories within these habitats. In addition, Eyre et al. (2003) recorded 182 instances of 46 rare United Kingdom beetle species within postindustrial vacant land sites, many of which are associated with natural habitats such as chalk grasslands, riverine sediments, pond edges, and sandy heaths. The streaked bombardier beetle, Brachinus sclopeta (F.), was rediscovered in the United Kingdom in a brownÞeld site (Jones 2006). Furthermore, Tropek et al. (2008) recorded spider and ground beetle assemblages within abandoned urban quarries in the Czech Republic as quite different from neighboring seminatural habitats and consisting of numerous region¨ ckinger et al. ally rare spiders. In urban Sweden, O (2009) reported approximately two more butterßy species (out of a total 17 in the study habitats, including highly managed parks) in previously industrial, early successional grasslands compared with seminatural grasslands. Recently, Woods (2012) documented the distributions of several rare moth species using both native and invasive plant species across vacant land sites in the Tees Estuary in the United Kingdom. This plethora of information highlights the importance of vacant land in urban areas for conservation of arthropod biodiversity. Further, to evaluate their conservation value, additional research into how vacant lot communities compare with those found in other urban and rural seminatural green spaces is clearly needed. Vacant Land Succession and Arthropod Communities The vegetation within temperate vacant land will, if left unmanaged, transition from pioneer vegetation to perennial herbs and grasses, and over time will incorporate shrub and tree cover (Small et al. 2003, Strauss and Biedermann 2006). This changing vegetation structure has a signiÞcant impact on arthropod communities (Small et al. 2003; Strauss and Biedermann 2006, 2008). Strauss and Bierdermann (2006) found that vegetation structure, including vegetation height and proportions of litter and moss cover vs. bare soil, were signiÞcant predictors of the species composition of leafhoppers and grasshoppers occupying vacant lands. The majority of species responded to intermediate values of vegetation structure; however, significant variations in species responses were reported. Strauss and Bierdermann (2006) note that pioneer species such as the leafhoppers Macrosteles quadripunctulatus (Kirschbaum) (Homoptera: Cicadellidae) and Psammotettix alienus (Dahlbom) (Homoptera: Cicadellidae) were restricted to early successional sites with low vegetation and a high proportion of bare soil. This contrasts to other taxa that were most abundant in sites with medium to high vegetation height, density, and litter or moss cover, and a low proportion of bare soil.

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Strauss and Biedermann (2006) maintain that the regional species pool of a city requires a mosaic of all successional stages of vacant land patches. The impacts of successional plant community change on ground dwelling predators, principally carabid communities, have also been studied within urban vacant land (Lazenby 1983, 1988; Weigman 1987; Anderson 2000; Eyre et al. 2003; Small et al. 2003). Successional changes inßuence several aspects of carabid assemblages. Small et al. (2003) found that the carabid communities shift from open habitat drytolerant and seed-feeding species to moisture-requiring species as successional changes occurred. Species found in early successional vacant lands were generally smaller with long thin legs facilitating rapid dispersal whereas later successional habitats favored larger species with adaptations for burrowing. The ßoral diversity found in early successional vacant lots also favored a greater abundance of Amara and Harpalus spp., many of which are seed feeders, whereas later successional habitats favored a community dominated by predatory carabids (Small et al. 2006). Human Perception of Vacant Land Despite the potential value of early successional vacant land, the appearance of these habitats (Fig. 2A) within cities can be negatively perceived by residents and city ofÞcials. In a study of visual preference for management alternatives within a highly industrialized area, Lafortezza et al. (2008) found that unmanaged early successional vacant land was the least preferred, with preferences for alternative greening strategies dependent on the participantsÕ relationship to the land (i.e., industrial employee or stakeholder) and the distance they live from the site. The preferred management strategies are typically managed complex habitats able to support a high diversity of organisms. Moreover, Fuller et al. (2007) demonstrated that the psychological beneÞts green spaces offered to residents increases with the plant species richness of the habitat. These studies suggest that management strategies to enhance plant species richness of vacant land can simultaneously increase ecological function and personal well-being of local citizens. In addition to affecting the individual, the perception of unmanaged or abandoned habitats can have signiÞcant consequences for entire neighborhoods. For example, Branas et al. (2011) found that the design and maintenance of vacant land impacts human community health and safety. The Pennsylvania Horticultural Society and several community partners adopted vacant lots across four of Þve sections of Philadelphia, PA (the Northeast section was excluded as it contained ⬍0.2% vacant lots) and removed trash and debris, planted trees and tuft grass, and bordered each lot with a split-rail fence (Fig. 2). In a comparison of these managed sites with unmanaged vacant lots, Branas et al. (2011) found that this management was negatively associated with gun assaults and positively associated with reduced stress and increased exercise

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Fig. 2. The development of management plans for vacant land can have social, ecological, and economic consequences. The Pennsylvania Horticultural Society has worked with several community organizations to transform (A) successional vacant land plots to (B) managed green spaces. In this case, researchers found that the management efforts reduced crime and stress among residents in the surrounding neighborhood (Branas et al. 2011). (Photographs courtesy of the Pennsylvania Horticultural Society.) (Figure in color online.)

among residents. Branas et al. (2011) argue that crime rates decreased because tended lots were associated with a more watchful community. Managed greening of vacant lots also offered health beneÞts, with residents reporting that a safe haven to enjoy outdoor activity reduced stress and provided opportunity to exercise (Branas et al. 2011). For ecologists, these Þndings offer a clear reminder of the complexity involved in designing habitats for vacant land management. Designing and Managing Multifunctional Urban Green spaces A challenge in the management of urban landscapes is the level of multifunctionality and diverse ecosystem services desired of green spaces (Bolund and Hunhammer 1999, Lovell and Johnston 2009). Vacant

land redesign and management needs to consider how tactics aimed at environmental concerns, such as supporting biodiversity or improving inÞltration of storm water, affects residents living within the targeted neighborhood. Altered maintenance costs resulting from the adoption of one or more of these strategies can be estimated, but predicting the ecological and social impacts of these land-use decisions is more complex. For example, there is the potential to introduce ecosystem disservices through vacant land management (Lyytima¨ki and Sipila¨ 2009). The presence of abandoned dwellings and vacant land in cities alters the suitability of a landscape for many species including those considered a nuisance (Fig. 3). Thus, an approach that considers the positive and negative impacts of management decision-making is not only necessary but essential to maintain the long-term sustain-

Fig. 3. As humans move out of a neighborhood, the presence of abandoned dwellings and vacant land alters the breeding and foraging resources available for wildlife, including species considered a nuisance. For example, (A) animals may create burrows in basements and under porches of abandoned homes, and (B) tire dumping creates breeding habitat for mosquitoes. Therefore, as vacant land ecosystem management plans are developed, it is important to consider potential ecosystem disservices that could result. (Figure in color online.)

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Fig. 4. In Cleveland, OH, vacant land is seeded with a turfgrass seed mix after demolition of abandoned or foreclosed structures. (A) Vacant sites are mown monthly during the growing season. In addition to the planted turf, common weedy grass and forb species such as Poa annua, Digitaria ischemum, Trifolium repens, Trifolium pretense, and Plantago lanceolata (Grewal et al. 2010, Yadav et al. 2012, Gardiner et al. 2013) are found within the managed interior of the site. (B) Unmanaged edges of vacant lot habitats contain a diverse mix of perennial herbs, shrubs, and trees planted by previous residents as well as native and nonnative colonizers. (Figure in color online.)

ability of ecosystem beneÞts, services, and resources (Zipperer et al. 2000). Considerations for Vacant Land Greening Initiatives. The dissemination of information pertaining to vacant land management is critical, as some cities are faced with responsibilities for increasing acreage and may have to reevaluate current management plans in the near future. Currently, in Cleveland, OH, a turfgrass seed mix is planted after the demolition of vacant homes and businesses, which is then mown monthly throughout the growing season (Fig. 4). These habitats contain remnant species established by previous landowners within unmanaged edges, and include common weedy grasses and nonnative and native ßowering plants within both the habitat edge and managed interior (Grewal et al. 2010, Yadav et al. 2012, Gardiner et al. 2013; Fig. 4). Managing vacant land by mowing can enhance its value for biodiversity. Kattwinkel et al. (2011) found that vacant land subject to periodic disturbance supported a greater diversity of species than undisturbed successional sites. They discussed management options, such as mowing, to preserve early successional patches within the urban mosaic (Kattwinkel et al. 2011). In addition, Angold et al. (2006) noted that the greatest ßoral diversity in vacant lot sites occurs when they are young, with convergent succession evident over a 20-yr period, which may support a greater diversity and abundance of beneÞcial species that use ßoral resources. Despite the potential beneÞts of this strategy for arthropod biodiversity, when vacant land acreage increases and budgets decline, it may become logistically and economically difÞcult to sustain frequent

mowing. The cost to manage vacant land currently exceeds US$3 million annually in Cleveland (Community Research Partners and ReBuild Ohio 2008). Several alternative strategies for vacant land management are currently being examined, including “no mow” groundcovers consisting of fescue grasses alone or in combination with low-growing forbs, plantings of native or nonnative tall grasses, forbs, shrubs and trees, and ornamental and food gardens or farms managed by individuals, organizations, or communities. Some of these alternatives have been installed on vacant lots by community organizations, food gardens and farms being the most common, but others such as native “pocket prairies” have also being incorporated into city landscapes (Fig. 5). Studies of Urban and Suburban Green Spaces Inform Vacant Land Management. Several studies within urban and suburban managed green spaces provide evidence of how changes in plant community composition affect, and also are altered by, arthropods and the ecosystem functions and services they supply. Factors such as patch size, shape, productivity, and vegetation composition and diversity can inßuence arthropod communities and their activity in urban landscapes (Hanks and Denno 1993; Shrewsbury and Raupp 2000, 2006; Tooker and Hanks 2000; McIntyre et al. 2001; Shrewsbury et al. 2004; Bolger et al. 2008; Pinna et al. 2009; Pecarevic et al. 2010; Raupp et al. 2010; Hennig and Ghazoul 2011). The ornamental plants established within urban landscapes are dominated by nonnative species (Tallamy 2004), and many were selected for their pest resistance, which can impact herbivore biomass and urban arthropod food webs (Tallamy 2004, Raupp et al. 2010). Several stud-

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Fig. 5. Several strategies for vacant land management are currently being examined by cities facing the high cost of monthly mowing during the growing season. (A) The organization Re-Imagining Cleveland provides grant funding to neighborhood groups, churches, schools, and individuals to carry out vacant land reclamation projects. (B) These projects include pocket prairies, where native plants take the place of managed turfgrass. Measuring the value of these urban native grasses and forb plantings to enhance rare, threatened, and beneÞcial arthropods is a key area for future research. (Figure in color online.)

ies have demonstrated a higher attractiveness of native vs. nonnative plants to arthropod predators, parasitoids, and pollinators (Fiedler and Landis 2007a,b; Fiedler et al. 2008; Frank et al. 2008; Tuell et al. 2008). Further, landscaping with native vs. nonnative plants has been shown to support a greater diversity and abundance of some arthropods including larval Lepidoptera, native bees, and honeybees in suburban residential sites and urban gardens (Frankie et al. 2005, Burghardt et al. 2009). However, establishing native plants does not always result in enhanced arthropod foraging. For example, Matteson and Langellotto (2011) found that nonnative ornamental plants were more frequently visited by megachilid bees and butterßies in New York City community gardens. In addition to species selection, the overall diversity and structural complexity of planted habitats can inßuence arthropod communities in urban landscapes (Shrewsbury and Raupp 2000, 2006; Raupp et al. 2001, 2010; Smith et al. 2006; Frankie et al. 2009). Raupp et al. (2001) found that the diversity and abundance of herbivores increased with plant species diversity in the landscape. However, increasing landscape plant diversity often decreases the severity of pest outbreaks (Hanks and Denno 1993; Trumbule and Denno 1995; Shrewsbury and Raupp 2000, 2006; Tooker and Hanks 2000). For example, Shrewsbury and Raupp (2006) found a specialist exotic herbivore, the azalea lace bug, Stephanitis pyrioides (Scott) (Hemiptera: Tingidae), was 120 times more abundant in simple vs. complex habitats. Total predation pressure was greater in complex habitats where a greater abundance of alternative prey were found, in turn supporting the hunting spider, Anyphaena celer (Hentz) (Araneae: Anyphaenidae), which served as a key natural enemy (Shrewsbury and Raupp 2006). Similarly, Tooker and Hanks (2000) found that simple habitats where pines were surrounded by mulch or an impervious surface had greater scale abundance compared with those planted in park-like settings where pred-

ators tend to be more numerous in the surrounding vegetation.

Vacant Land Within an Urban Landscape Context Given the increasing acreage of vacant land in many cities, alteration of plant communities within these habitats could result in landscape-scale consequences for a cityÕs ecology. Several studies have considered how landscape composition and conÞguration inßuences arthropod communities within the context of urban-to-rural gradients (e.g., Mcdonnell and Pickett 1990, Denys and Schmidt 1998, Alaruikka et al. 2002, Ahrne´ et al. 2006, Bates et al. 2011, Bennett and Gratton 2012). The concept of the urban-to-rural gradient describes urbanization as a large-scale disturbance that inßuences a variety of factors including building and pavement development, habitat isolation and fragmentation, pollution levels, and plant diversity because of direct human management. Such changes can be measurably different along urban-to-rural gradients and have been demonstrated to impact a variety of arthropods and their ecosystem services. For example, Bates et al. (2011) found bee and hoverßy pollinator communities to be more diverse and abundant in rural churchyards and cemeteries in Birmingham, United Kingdom, compared with urban sites that had lower ßowering forb species richness and higher degrees of built space in their surrounding landscape. Similarly, bumble bee diversity in United Kingdom allotment gardens decreased with increasing urbanization of the surrounding landscapes (Ahrne´ et al. 2009). Denys and Schmidt (1998) measured urbanization as proportion of built area and found herbivores and their natural enemies decreased in diversity in potted mugwart (Artemisia vulgaris L. (Asterales: Asteraceae)) plants as the proportion of built areas increased. Conversely, Alaruikka et al. (2002) found no gradient differences in forest carabid beetle or

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Fig. 6. Urban agriculture is growing worldwide in cities. Formerly vacant land currently supports local food production for personal consumption and for-proÞt sale. Production occurs at scales ranging from (A) community gardens managed by neighborhood residents to (B) market gardens and community-supported agriculture production systems covering 1 ⫹ city block(s). (Photograph B courtesy of Carl J. Skalak, Blue Pike Farm, Cleveland, OH.) (Figure in color online.)

spider diversity, but urban carabids tended to be smaller and less habitat-specialized. Other studies have focused on a smaller spatial scale where city landscapes are composed of a mosaic of green spaces and potential habitat for arthropods. Urban areas consist of a variety of habitat types, including natural habitat remnants, private and city gardens, managed grass courtyards in areas of industry, and vacant lands (Shochat et al. 2004, Sattler et al. 2010, Faeth et al. 2011, Snep et al. 2011, Vergnes et al. 2012). These green spaces experience different levels of disturbance and harbor varying plant species, both of which inßuence arthropods and the services they can supply within and between patches. For example, Sattler et al. (2010) found urban patches within more diverse mosaics were correlated with richer phytophagous and pollinator assemblages, most likely because of the proximity of habitats and the arthropodsÕ ability to recolonize from neighboring locations. Thus, by adding to the amount of green space within a mosaic, vacant lots have the potential to aid conservation and enhance green space quality and connectivity within city centers (e.g., Snep et al. 2011). A Changing Urban Landscape—Vacant Land for Local Food Production As ecologists work to understand how green space design and management affects ecosystem functions and services, one major initiative is already underway using vacant land. Local food production in cities addresses food insecurity, which affects ⬇49 million people in the United States and contributes to both hunger and obesity because of a lack of access to healthy food options (Pothukuchi and Kaufman 1999, Corrigan 2011). Access to nutritious food is especially limited in low-income communities, where many residents lack access to personal or public transportation or supermarkets within walking distance that carry fresh produce (Moreland et al. 2002). Community food security is a strategy to ensure that community

members obtain food through safe and culturally acceptable means, incorporating environmentally sustainable techniques in an economically sound manner (Hamm and Bellows 2003). The incorporation of local food production in cities is an important component of community food security (Corrigan 2011). Farming in urban environments is growing rapidly with community gardens, market gardens, and small scale polyculture farms being incorporated into the landscape. Production occurs at several scales from single vacant lot community gardens to farms extending more than a city block in size (Grewal and Grewal 2012; Fig. 6). Many cities have adopted policies allowing for the production of crops, as well as animal products such as honey and eggs, in support of improving community nutrition. Therefore, urban agriculture can provide a diversity of new employment opportunities and increased access to locally produced products (Blaine et al. 2010, Grewal and Grewal 2012). These sites require the work of beneÞcial insects including natural enemies and pollinators to produce crops sustainably. For example, Matteson and Langellotto (2009) report that 92% of crops commonly grown in New York City community gardens require or beneÞt from bee pollination services. The enthusiasm of many communities to incorporate farming into cities offers an opportunity for researchers to advance current knowledge of how local disturbances (i.e., gardening and farming practices) and landscapescale composition and heterogeneity inßuence the supply of beneÞcial insects and their ability to suppress herbivorous pests and provide pollination in an urban environment. Arthropods in Vacant Lots vs. Those Converted to Urban Agroecosystems. Several studies have compared arthropod communities and their activity in vacant lots and lots converted to urban gardens or farms. Research conducted in Akron, Cleveland, and Toledo, OH, and Detroit, MI, found similar abundances or activity densities of several above-ground and ground-dwelling natural enemy groups (Uno et al.

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2010, Gardiner et al. 2013). For example, Uno et al. (2010) found that ant activity density did not differ among vacant lots and gardens, and both habitats had twice the activity density found in urban forests (Uno et al. 2010). However, ant species richness was greater within urban forests than community gardens while vacant lots were intermediate in richness and did not differ from the other habitat types (Uno et al. 2010). Gardiner et al. (2013) also found similar ant activity densities among community garden and vacant lot habitats. Several other agriculturally important generalist predators including Carabidae, Coccinellidae, Lycosidae, and Syrphidae were as abundant, and Anthocoridae and Staphylinidae were more abundant within community gardens relative to vacant lot habitats in Cleveland, OH (Gardiner et al. 2013). Conversion of vacant land to community gardens can negatively impact some predatory arthropod groups. For example, Friedrich and Philpott (2009) found that vacant lots supported nearly twice the number of natural cavity-nesting ant colonies compared with community gardens (76 vs. 39 nests collected); both habitats supported fewer nesting sites relative to urban forests. By placing artiÞcial nests within each of these habitats, Friedrich and Philpott (2009) found that nests within garden sites were not colonized, which was attributed to low source populations. Gardiner et al. (2013) found that the abundance of long-legged ßy (Dolichopodidae) adults and activity densities of sheetweb weaver spiders (Linyphiidae) and Opiliones were reduced in community gardens relative to vacant lots in Akron and Cleveland, OH. Although the functional roles of Dolichopodidae have not been studied extensively, they do feed on several agricultural pests (Ulrich 2004). The value of arachnids for biocontrol services is well established, and these losses likely have implications for sustainable crop production (Riechert and Lockley 1984, Nyffeler 1999, Harwood et al. 2004, Harwood and Obrycki 2007). Disturbances created in the establishment and maintenances of gardens and urban farms may be driving these changes in arthropod abundance and activity density. Community garden sites may not have regulations on the use of pesticides by gardeners, and urban farms can follow organic or conventional pest management practices. To date the frequency of pesticide use and its impact on beneÞcial organisms within these habitats have not been examined. Changes in soil structure have been found, with vacant lots reported as being lower in moisture, organic matter, and nitrate-nitrogen than community gardens, which is likely because of soil tillage and irrigation and the addition of compost and fertilizer (Grewal et al. 2011). These changes could also result in part from the addition of soil to garden sites. Garden construction also reduced soil food web productivity, as indicated by reduced total nematode abundance, free-living nematode abundance, and the number of nematode genera found. These soil food webs inßuence sustainable food production through the maintenance of supporting services including decomposition of organic

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matter, nutrient and mineral cycling, carbon sequestration, detoxiÞcation of pollution, and biological control of below-ground pests (Grewal et al. 2011). However, these appear to be short-term impacts, as established gardens (15Ð30 yr of cultivation) and vacant lots in Cleveland, OH, had similar nematode communities (Grewal et al. 2011). Biocontrol Services Within Vacant Lots and Urban Agroecosystems. Changes in species richness, abundance, or activity density of particular natural enemies may translate to changes in the levels of biocontrol services provided within urban habitats. Yadav et al. (2012) and Gardiner et al. (2013) measured the levels of biocontrol services provided to vacant lots and community gardens using sentinel or indicator prey. Yadav et al. (2012) measured below-ground biocontrol services using waxworm [Galleria mellonella (L.) (Lepidoptera: Pyralidae)] as an indicator species. They reported 51Ð98% mortality after 48 h of exposure in the Þeld, and detected reduction in biocontrol within community gardens (Yadav et al. 2012). Differences in the composition of the community attacking G. mellonella larvae were also detected between gardens and vacant lots. Ants provided a greater proportion of total biocontrol services in vacant lots whereas microbial pathogens contributed signiÞcantly to pest suppression in community gardens (Yadav et al. 2012). Thus, land use changes can alter the contributions of organisms to key ecosystem functions within these managed green spaces. Gardiner et al. (2013) used eggs of Helicoverpa zea (Boddie) (Lepidoptera: Noctuiidae) and pupae of Sarcophaga bullata Parker (Diptera: Sarcophagidae) and Musca domestica L. (Diptera: Muscidae) as indicators of above-ground and ground-level biocontrol service. Generalist predators signiÞcantly reduced the abundance of all indicator prey present within both garden and vacant lot habitats. Overall, predatory function was maintained within community gardens relative to vacant lots (Gardiner et al. 2013). Seasonal patterns emerged across sites with implications for crop production. The extent of egg biocontrol supplied within the community gardens and vacant lots was low in early summer but increased late in the growing season. Early season arrival of predators and parasitoids into agroecosystems, before pests reaching outbreak levels, is key to successful herbivore suppression (Landis and Van der Werf 1997; Harwood et al. 2004, 2007; Bianchi et al. 2006). Building on these studies, examination of crop-speciÞc pest-natural enemy interactions and the impact of biocontrol services on food system sustainability is a key area for future research. Pollinators and Pollination Services. Urban community gardens can support a diverse and abundant arthropod pollinator community (Matteson et al. 2008, Matteson and Langellotto 2010). Matteson et al. (2008) found 54 bee species within New York City community gardens, the most abundant being two exotic species (Hylaeus leptocephalus Morawitz and Hylaeus hyalinatus Smith (Hymenoptera: Colletidae)) and the native bumble bee Bombus impatiens

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Cresson (Hymenopera: Apidae). The majority of bees collected were solitary or communal, polylectic, and were either soil or cavity nesters (Matteson et al. 2008). Matteson et al. (2008) noted that a much larger percentage of their collection was composed of exotic taxa than studies from outside urban areas (exotics made up 19% of the species and 27% of the individuals collected). In addition to higher numbers of exotic species, the proportion of cavity-nesting bees was also higher in urban sites. The presence of impervious surface area in the urban habitat likely selected against soil-nesting species. Within the same garden system, Matteson and Langellotto (2010) found 24 species or taxa of butterßies and 54 species of bees, with richness of both taxa positively related to sunlight availability and garden ßoral area. Bee species richness was also correlated with garden area, canopy cover, and the presence of wild and unmanaged areas. Matteson and Langellotto (2010) attributed relationships to local habitat variables to the varied life histories of butterßies and solitary or communal bees. Butterßies are highly mobile and use gardens as a foraging habitat, whereas cavity- and soil-nesting bees may, in addition, use unmanaged areas within garden sites for nesting (Matteson and Langellotto 2010). Fewer studies have compared the diversity and abundance of foraging pollinators among vacant lots and lots converted to agriculture. A preliminary survey documented 16 genera of bee pollinators from pan traps placed within Akron and Cleveland, OH, vacant lots and community gardens in July 2009, with a similar abundance of syrphid and bee pollinators, and pollinator diversity, recorded among the green spaces (S.P.P., unpublished data). Further work needs to examine how vacant land conversion into agriculture inßuences both foraging and nesting resources within the urban environment, as well as the pollination services provided. As pollinators are currently undergoing worldwide declines because of habitat loss, pesticide exposure, and disease, it will be important to continue evaluating how stressors associated with vacant land conversion affects pollinator health and pollination services. Enhancing Beneficial Insects in Urban Agroecosystems. Researchers are also beginning to examine methods of habitat management that encourage beneÞcial arthropods within urban agroecosystems. Gaston et al. (2005) found stem-nesting blocks added to urban gardens were colonized by bees, but it was unclear whether providing these resources resulted in increased richness or abundance of bee fauna within garden sites. Matteson and Langellotto (2010) measured how the addition of native plants to urban food gardens in New York City inßuenced predators and pollinators. They found that an additional planting of 70 native plants of seven species to community gardens did not increase the species richness of bees, predatory wasps, or butterßies (Matteson and Langellotto 2010). Matteson and Langellotto (2010) surmised this could be because of the plants not addressing nesting needs or that the 10-m2 area of plants added to each site may have been insufÞcient to in-

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crease species richness. In addition, garden sites initially supported high richness and abundance of ßoral resources, which may have already attracted the species pool present within the surrounding landscape. A lack of a preference for native plants may also be because of the generalist feeding habitats of the majority of arthropods within the New York City landscape sampled (Matteson and Langellotto 2011). Future Research Within Vacant Land Green Spaces The study of vacant land ecology necessitates a transdisciplinary approach that considers how alteration of plant communities occupying signiÞcant acreage within urban landscapes will affect diverse ecosystem functions and services. No single management strategy will provide the ideal green space for every former residential and commercial vacant land parcel found within a city. Thus, managers need tools to rapidly assess their vacant lot inventory and determine the most appropriate strategies for improving the sustainability of cities from a connected landscape perspective. To date, efforts to redesign declining neighborhoods have not fully considered the ecological implications of the many alternative management options. Ecological theory can guide revitalization by examining how the changing spatial pattern of a city inßuences its ecological structure and function. As the urban landscape is highly fragmented, the equilibrium theory of island biogeography (MacArthur and Wilson 1967) and metapopulation theory (Hanski 1998) are often applied to understand its dynamics. Both suggest that habitat fragmentation increases the probability of extinction within an isolated habitat patch and reduces the likelihood of recolonization of the patch by individuals from remaining populations. Thus, the amount, arrangement, and habitat quality of vacant land are likely to be key drivers of arthropod community composition and function. Patch dynamics (Wu and Loucks 1995, Pickett and Rogers 1997) reÞnes these theories by recognizing that the landscape matrix surrounding habitat patches is not homogenous. Patch dynamics from a landscapeecology perspective has been applied at multiple scales to study changing cities (Grimm et al. 2000; Pickett et al. 2001, 2011; Swan et al. 2011). Spatial patchiness can be deÞned and quantiÞed in terms of both patch composition (habitat types and their relative abundance) and spatial conÞguration (habitat size, shape, edge characteristics, and landscape context; Wu and Loucks 1995). The change of individual patches at local scales (Þne-scale patchiness within vacant lands) and the pattern change in patch mosaics at broader scales give rise to system dynamics. The theory of patch dynamics proposes that the distribution and abundance of species within a landscape are inßuenced by its heterogeneity, with individual patches supporting different communities of species and the mosaic of patches within a landscape inßuencing the ßow of materials, energy, and organisms (Pickett and Rogers 1997). Therefore, shifting the

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species composition of plant communities within vacant land patches could inßuence the number of taxa occupying higher tropic levels, food web connectivity, and the provision of ecosystem functions and services (Symstad 2000; Haddad et al. 2001, 2011; Duffy 2002; Faeth et al. 2011). As vacant land acreage grows in cities like Cleveland, OH, evaluating the inßuence of patch size, composition, and connectivity on biodiversity and ecosystem function relationships is critical (Cardinale et al. 2006, Duffy et al. 2007, Loreau 2010). Clearly many alternative compositional outcomes for vacant land are possible and urban revitalization projects often aim to enhance biodiversity across many trophic levels. An assumption driving these projects is that establishing diverse plant communities will support greater richness at higher trophic levels and enhanced ecosystem functions and services (Srivastava and Vellend 2005). However, without understanding the mechanisms responsible for predicted biodiversityÐ ecosystem function patterns, the results of revitalization efforts are difÞcult to predict and hard to replicate even when desirable outcomes are achieved (Srivastava and Vellend 2005, Faeth et al. 2011). Therefore, a greater understanding of how patch-scale plant species and plant functional trait richness, evenness, and divergence inßuence communities and their interactions, will be critical for advancing our understanding of vacant land ecosystem functioning (Mason et al. 2005, Mouillot et al. 2005, Lavorel et al. 2008). Moreover, the landscape context of vacant land patches is also likely to mediate biodiversity and ecosystem function relationships (Wu and Loucks 1995, Fahrig and Nuttle 2005, Fahrig et al. 2011). The importance of these elements on populations and their interactions has long been recognized (MacArthur and Wilson 1967, Hanski 1998, Loreau et al. 2003) and extensively studied and applied in urban landscapes (Pickett et al. 2001, 2008; Alberti 2005; Lovell and Johnston 2009; Wiens 2009). Landscape variables clearly inßuence arthropod species richness, abundance, and activity (Mcdonnell and Pickett 1990, Blair 1999, Sattler et al. 2010). However, the mechanisms driving observed patterns are not fully understood and the role that vacant land growth and management may play in has not been evaluated. Further, a greater understanding of the ecological impacts of land-use legacy on vacant lot ecology is needed (Foster et al. 2003). A history of contamination within a sampled vacant land parcel or within the surrounding landscape may negatively impact the biota vacant land management seeks to attract and retain. Contamination of urban soils with lead and other heavy metals is a key human health concern (Clark et al. 2006) and may negatively affect arthropod communities as well. Uptake of heavy metals can occur via diet or contact with the body surface and will be inßuenced by many factors including an organismÕs tropic level and foraging strategy (Tyler et al. 1989). This exposure has been found to affect arthropod longevity and fecundity (Chen et al. 2011); however, the full spectrum of impacts that heavy metals and

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other contaminants may play in the structure and function of urban food webs is far from understood. In addition to environmental pollution, the potential ecological impact of pesticide use practices within urban agricultural production is a key area for future research. In addition, working within urban areas requires a focus on how climate inßuences communities and their interactions. Cities are subject to higher temperatures compared with rural landscapes; these “heat islands” result from a greater proportion of buildings, asphalt, and reduced vegetation cover (Kim 1992). Variation in temperature among urban microhabitats may alter the composition and function of arthropod communities in green spaces. For example, Meineke et al. (2013) demonstrated that abundance of the scale insect, Parthenolecanium quercifex (Fitch) (Hemiptera: Coccidae), was signiÞcantly higher in hotter areas of the urban ecosystem of Raleigh, NC, despite similar parasitism rates. Further greenhouse studies conÞrmed an adaptation of the scale to higher temperatures, as populations collected from urban trees within hotter microhabitats reached a greater abundance in hot greenhouses than cool greenhouses whereas scales collected from trees in cooler microhabitats remained low on plants held under both temperature regimes (Meineke et al. 2013). This study illustrates how vacant lot green space variables such as patch size and landscape context could result in microclimatic differences. The effects of climate variables on community composition and food web structure clearly necessitate additional research, as these could result in varied outcomes of vacant land ecosystem management. Addressing research questions regarding the ecology of vacant land within the framework of patch dynamics represents a signiÞcant opportunity to contribute to the Þeld of urban ecology. McIntyre (2000) outlined an argument for arthropods as key indicator of urbanization impacts, citing that they are diverse and occupy multiple trophic levels, respond quickly to anthropogenic change, and are easy to sample. These same characteristics support the study of arthropods to measure the impact of deurbanization on biodiversity, ecosystem function, and the provision of ecosystem services. Thus, entomologists have a key role to play in identifying the species within these parcels and determining how they move and function throughout a changing urban landscape. Acknowledgments We thank J.D. Harwood, the Agricultural Landscape Ecology Laboratory, and four anonymous reviewers whose feedback was very helpful in revising of an earlier draft of this manuscript. We thank the Ohio Agricultural Research and Development Center Research Internship Program for providing funding support for two high school students (Shanae´ Davis and Kojo Quaye) who conducted the pollinator survey described herein. We also thank our collaborators within the Cleveland Urban Long Term Research Area Exploratory (ULTRA-EX) Project funded by National Science Foundation as well as the Pennsylvania Horticultural Society for providing images. Funding sup-

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port for vacant land research was provided to M.M.G. by the National Science Foundation Division of Environmental Biology (CAREER 1253197) and the United States Environmental Protection Agency (Contract EP-C-12048-C).

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December 2013

GARDINER ET AL.: VACANT LAND SUPPORTS ARTHROPOD BIODIVERSITY

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The value of urban vacant land to support arthropod biodiversity and ecosystem services.

The expansion of urban areas is occurring globally, but not all city neighborhoods are gaining population. Because of economic decline and the recent ...
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