Insect herbivory on Acer rubrum varies across income and urbanization gradients in the D.C. metropolitan area

Insect herbivory on Acer rubrum varies across income and urbanization gradients in the D.C. metropolitan area | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Insect herbivory on Acer rubrum varies across income and urbanization gradients in the D.C. metropolitan area Elizabeth Blake, Shelley Bennett, Amy Hruska, Kimberly J Komatsu This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4219885/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 25 Jul, 2024 Read the published version in Urban Ecosystems → Version 1 posted 11 You are reading this latest preprint version Abstract Urbanization has increased wealth disparity within the United States, impacting the urban landscape and species interactions. In particular, the interactions between street trees and the arthropod communities that live among them may be modified by both human population densities across urban to suburban locations, as well as income levels within these areas. We examined the effect of land use type (urban vs suburban) and median household income on variation in leaf damage and arthropod abundance of red maples ( Acer rubrum ) in the District of Columbia metropolitan region. We compared these levels of leaf damage to rates observed in a nearby natural forest. We predicted leaf damage would be positively correlated with urbanization (forested < suburban medium > high). Instead, we observed higher levels of leaf damage on trees in the forest environment compared to the urban and suburban areas. Leaves from urban medium and high-income areas were less likely to exhibit herbivore damage than those from suburban areas. Of the leaves with any damage, those in urban high-income and suburban low-income areas exhibited the most leaf area missing. These trends may be related to specific factors associated with urbanization and income level, such as tree and impervious surface coverage and pesticide use. This study highlights differences in biotic interactions across individual neighborhoods and the importance of including socio-economic variables (e.g., household income) when examining species interactions in developed environments. land use urban suburban forest leaf damage red maple street trees Figures Figure 1 Figure 2 Figure 3 Figure 4 1. Introduction Trees are key components of many urban ecosystems. In particular, street trees are important for cities as they supply environmental, economic, and social benefits for their city’s residents (Donovan & Butry, 2010 ; Landry & Chakraborty, 2009 ; Mullaney et al., 2015 ; Soares et al., 2011 ; Wolf et al., 2020 ). Thus, urban planning must critically consider tree health (Alvey, 2006 ; Felson et al., 2013 ). While tree health is impacted by abiotic and biotic factors (Hilbert et al., 2018 ), herbivory in particular can have large consequences for tree growth, success, and survival (Crawley, 1989 ). Further, herbivory can impact ecosystem productivity by modifying nutrient cycling (Bagchi et al., 2014 ; Lamarre et al., 2012 ; Metcalfe et al., 2014 ). Urban street trees provide invaluable ecosystem services to their surrounding environment (Beecham & Lucke, 2015 ; Turner-Skoff & Cavender, 2019 ). For example, urban trees can serve as habitats for various species, increasing species diversity in urban ecosystems (Pataki et al., 2021 ). This being considered, it is important to understand how trees and their herbivorous residents are impacted by increasing urbanization (Lahr et al., 2018 ). On average, plants suffer greater effects from invertebrates than from vertebrate herbivores (Bigger & Marvier, 1998 ). While most damage from an individual herbivorous insect may be minor, collectively they can substantially damage plants, even at low densities (Kozlov & Zvereva, 2018 ). Herbivory results in tissue removal, which decreases leaf area and directly impacts photosynthesis, growth, leaf abscission, costly induced defenses, and leaf vulnerability to pathogens (Björkman et al., 2008 ; Kozlov et al., 2012 ; Kozlov et al., 2014 ; Marquis & Whelan, 1994 ). For example, sap-feeding herbivores can cause a reduction in chlorophyll content and decrease stomatal conductance, limiting photosynthesis and cell respiration (Cabrera et al., 1994 ; Kaakeh et al., 1992 ; Nabity et al., 2009 ; Schaffer & Mason, 1990 ). Similarly, root feeders disrupt water and nutrient uptake (Johnson et al., 2016 ), impacting photosynthesis by indirectly decreasing CO 2 availability and altering photosynthetic metabolism and oxidative stress (Chaves et al., 2009 ). While sap and root feeders play a part in plant health, it is estimated that 90% of leaf damage is due to externally feeding defoliators (Kozlov et al., 2015 ). Not only does foliar herbivory remove leaf tissue, but leaf damage has the potential to impact surrounding tissue (Nabity et al., 2009 ; Welter, 1989 ; Zangerl et al., 2002 ), further limiting photosynthetic capabilities. This cycle is further propelled as decreased photosynthesis can lead to reduced bud development and production of smaller leaves, which sets up a positive feedback loop by providing less support to subsequent buds, resulting in shorter shoots the following growing season (Zvereva et al., 2012 ). Thus, understanding the effects of foliar insect herbivory on urban trees is essential for promoting their health and maintenance. Previous research shows conflicting patterns related to herbivore abundance on trees in urban settings. There is little evidence for a universal increase in herbivore abundance or species richness along urbanization gradients, although guild-specific trends have been identified (Raupp et al., 2010 ). Specifically, Coleoptera (beetles) and Lepidoptera (butterflies and moths) tend to decrease in abundance, while Hemipterans (true bugs) often increase in abundance in cities relative to less urban environments (Schmitt & Burghardt, 2021 ). In their review, Raupp et al. ( 2010 ) found that most small arthropods with sucking mouthparts, limited mobility, multiple generations on the same host plant, or other intimate associations with hosts generally increase along an urbanization gradient. Understanding the consequences of these urbanization impacts on herbivore abundances and community composition for plant damage levels is a critical knowledge gap. Existing studies that compare herbivory rates between urban and rural areas are conflicting, with some demonstrating that urban trees experienced higher levels of insect herbivory relative to rural habitats (Cuevas-Reyes et al., 2013 ; Turrini et al., 2016 ), while others found decreased herbivory in urban environments (Bode & Gilbert, 2015 ; Herrmann et al., 2012 ; Kozlov et al., 2017 ; Moreira et al., 2019 ). Although urbanization's effect on herbivory rates on street trees has been studied across several cities (Moreira et al., 2019 ), no studies have holistically considered how the economic characteristics of urban areas may impact herbivory. While FDR’s New Deal attempted to boost the economy during the Great Depression, it ended up having lasting effects on communities’ racial and socioeconomic makeup; redlining and restricting people of a certain race or class to specific neighborhoods became common (Young, 2010 ). Formerly redlined neighborhoods are less developed by the city, often lacking infrastructure and green space, which leaves already vulnerable populations exposed to higher temperatures due to the urban island heat effect and a variety of other environmental threats (Chakraborty et al., 2019 ; Hoffman et al., 2020 ; Hsu et al., 2021 ). Thus, it is not representative to group together all neighboring communities within a city when examining plant-herbivore interactions, as these communities can vary significantly due to the impacts of segregation on the urban landscape’s features and characteristics. The lack of nuanced studies considering income gradients in addition to urbanization level may explain the discrepancies we currently see in the literature regarding the role of urbanization on herbivory rates. Red maple ( Acer rubrum ) is native to and ubiquitous across the eastern United States (Walters & Yawney, 1990 ) and is a popular street tree species planted for its generalist nature and ability to grow in a range of soil conditions (National Wildlife Federation). Despite how abundant and widespread red maple is, few studies have focused specifically on red maple in an urban context. The limited research that exists demonstrated that red maple was negatively impacted by urban warming (Dale & Frank, 2014a , 2014b ) due to increased fecundity, abundance, and survival of the gloomy scale ( Melanaspis tenebricosa ) on these trees (Dale & Frank, 2017 ). In this study, we examine 1800 red maple leaves to determine whether herbivory levels vary along an urbanization gradient and across income levels within urbanization types in the D.C. metropolitan area. We compared herbivorous insect chewing damage on leaves of red maple in the District of Columbia; Montgomery County, Maryland; and the natural forested area of the Smithsonian Environmental Research Center (SERC) in Edgewater, Maryland. We sought to determine whether leaf damage on red maple varies along the urbanization gradient, with the expectation that leaf damage will be positively correlated with urbanization (urban > suburban > forested). We also examined whether income level within urban and suburban areas impacts leaf damage or arthropod abundances. We predicted a negative relationship between arthropods abundance and neighborhood income levels, with arthropod abundance and herbivory being inversely related to income due to increased temperatures and heat stress (low > medium > high income). 2. Methods 2.1. Study Sites The D.C. Metropolitan area encompasses the District of Columbia (D.C.) and surrounding Maryland and Virginia suburban areas. Here we focus on sites in the District of Columbia, Montgomery County, Maryland and Anne Arundel County, Maryland. Study sites were selected based on red maple presence and categorized based on green space, percent pavement cover, and income. Sites were grouped into urban (District of Columbia), suburban (Montgomery County), and natural forested areas SERC (Anne Arundel County). Within the urban and suburban locations, three neighborhoods were chosen to span median household income levels (Fig. 1 ; Table 1 ). Census data were used to determine the median household income of the various census block groups of the sites, with classification into high, middle, and low-income were adapted from census-designated income brackets: high-income ( $ 121,000 and up), middle-income ( $ 84,000 - $ 121,000), and low-income ( $ 48,600 - $ 84,000) (Table 1 ). Within D.C. (urban), the Anacostia (low-income), Brightwood (middle-income), and Georgetown (high-income) neighborhoods were included in this study. In Montgomery County (suburban), the White Oak (low-income), Rockville (middle-income), and Travilah (high-income) neighborhoods were sampled in this study. To compare the levels of herbivory observed in the human-dominated areas to a natural forest, three sites within the 2650-acre forested grounds of the Smithsonian Environmental Research Center (Anne Arundel County, Maryland) were also selected for sampling (Fig. 1 ). Table 1 Table of neighborhood characteristics for each of the six human-dominated study sites. Anacostia [Urban, Low-Income] Brightwood [Urban, Mid-Income] Georgetown [Urban, High-Income] White Oak [Suburban, Low-Income] Rockville [Suburban, Mid-Income] Travilah [Suburban, High-Income] Area (sq mi) 1.6 0.8 1.1 5.2 0.7 10.4 Population Size 4,086 11,823 9,495 19,426 3,281 5,800 Median Household Income $ 53,501 $ 77,055 $ 178,756 $ 104,580 $ 124,821 $ 250,001 Percent Below Poverty Level 21.6% 11.6% 8.9% 10.1% 3.9% 1.4% Tree Coverage 34% 21% 30% 53% 56% 63% Impervious Surface Coverage 50% 60% 62% 27% 20% 7% 2.2 Study Species Red maple was chosen as a study species, as it is abundant across land-use types in the study region and the Northeast United States. In July of 2021, we sampled 10 red maple trees at each of our 9 study sites (N = 90 trees across all sites). Trees in each area were selected haphazardly, ensuring no directly neighboring trees were sampled. Each tree was roughly divided into four quadrants for sampling the arthropod community (urban and suburban sites) and herbivorous insect foliar damage (all sites). 2.3 Arthropod Collection Within the urban and suburban sites, we utilized a 91.44 x 91.44 cm beat sheet to collect arthropods from each of the four quadrants of each sample tree, utilizing a 30 ft pole to beat the branches in the quadrant for 15 seconds (1 minute total per tree). Arthropods that fell from the tree were collected from the beat sheet using an aspirator and placed into labeled collection tubes. Total arthropod abundance per tree was based on the summing of abundances found in each quadrant. Arthropods were not sampled from the natural forest sites due to the inaccessibility of tree branches. The arthropods were sorted into herbivores and predators based on broad taxonomic groupings using protocols developed by the Herbivory Variability Network (The Herbivory Variability Network et al., 2023 ). Herbivores identified included: grasshoppers/crickets/katydids, caterpillar-like, hoppers, aphids, thrips, mirid, mites, herbivorous beetles, and whiteflies/mealybugs/scale insects. Predators identified included: wasps, spiders, assassins, and predator beetles. 2.4 Leaf Collection Twenty leaves were randomly selected each of red maple (N = 1800 leaves in total), with five leaves collected within each of the four quadrants of each tree. Using a 30-foot extendable pole pruner, leaves were randomly selected from branches at various heights and different distances from the tree’s trunk to provide a comprehensive sample of each entire tree. To ensure the leaves suffered no additional damage after collection, all leaves were carefully placed in bags labeled by the site/tree number, placed in a cooler for transport to the lab, and kept refrigerated until processing. Photos of all leaves were taken within a week of collection and uploaded into the LeafByte application (Getman-Pickering et al., 2020 ), which we used to estimate percent leaf damage due to herbivory. In some cases, when large sections of the leaf were missing, we made an educated guess of the original outlines of the leaf, and the percent missing was then calculated with this supplemented information. In addition, great care was taken to ensure only herbivory was considered. Instances of tissue loss due to fungal infection, tearing, wind, or sun damage were excluded from the total percentage using the exclude feature in the LeafByte application. Percent damage was recorded for all leaves in the sample set. 2.5. Statistical Analysis All statistics were completed in R version 4.1.3. Leaf damage data were continuous and highly zero-inflated. As such, we conducted two-stage mixed-effects models using the lme4 package (Bates et al., 2015 ) to examine the effects of (a) land use type, including all data from forest, suburban, and urban sites, and (b) interactive effects of land use and income for the suburban and urban sites only. These two-stage models consisted of first examining the probability of observing zero values for percent leaf damage using logistic regression with a binomial distribution and including land use or land use by income interactions, as appropriate, as fixed factors and tree identity as a random effect. Then we examined the non-zero continuous data using a second model with log-transformed percent leaf damage as the dependent variable, land use or land use by income interactions, as appropriate, as fixed factors, and tree identity as a random effect. Herbivore and predator count data were analyzed for the suburban and urban sites only using the glmmTMB package (Brooks et al., 2017 ), including land use by income interactions as fixed factors, tree identity as a random effect, and using a single zero-inflation parameter and a negative binomial distribution. 3. Results 3.1 Leaf Damage by Area Type and Income Roughly 35% (635 of 1800 leaves) of leaves sampled experienced zero damage. Land use significantly affected the incidence of leaf herbivory, with a significantly higher probability of zero damage on urban leaves than suburban leaves and the lowest probability of zero damage on forest leaves (Fig. 2; x 2 = 227.24, df = 2, p < 0.001). Of the leaves with any damage, most damage values were low, with 45% (526 leaves) of damaged leaves having less than 1% damage and an additional 53% (614 leaves) of damaged leaves having between 1–20% damage. When considering leaves with damage, urban and suburban leaves had significantly lower average percent damage than forest leaves (Fig. 2; x 2 = 8.07, df = 2, p = 0.018; means ± standard errors were as follows, Urban: 0.89% ± 0.12%, Suburban: 0.93% ± 0.09%, Forest: 1.23% ± 0.12%). Despite these average trends, urban and suburban leaves were more likely to experience very high levels of leaf damage (Fig. 2 ; 8 urban leaves and 13 suburban leaves experienced greater than 20% damage, compared to only 4 forest leaves with such high damage values). When considering only the urban and suburban sites, income significantly interacted with land use to impact percent leaf damage (Fig. 3 ). Specifically, a significantly higher probability of zero damage was observed for urban leaves in medium and high-income neighborhoods than low-income urban neighborhoods, and low and high-income suburban neighborhoods were less likely to have zero damage leaves than urban neighborhoods of any income level (Fig. 3 ; x 2 = 10.66, df = 2, p = 0.005). When considering leaves with damage, leaves from high-income suburban and low-income urban neighborhoods had significantly greater damage than leaves from all other neighborhoods (Fig. 3 ; x 2 = 37.41, df = 2, p < 0.001; means ± standard errors were as follows, Suburban Low: 0.78% ± 0.13%, Suburban Medium: 0.59% ± 0.10%, Suburban High: 1.56% ± 0.25%, Urban Low: 1.83% ± 0.35%, Urban Medium: 0.70% ± 0.16%, Urban High: 0.54% ± 0.13%). 3.2 Arthropods Abundance by Area Type and Income Across the urban and suburban sites, there was a significant interactive effect of land use and neighborhood income on invertebrate herbivore (x 2 = 148.50, df = 2, p < 0.001) and predator abundances (x 2 = 124.69, df = 2, p < 0.001). Specifically, herbivore abundances were lowest in the urban and suburban low-income neighborhoods (Urban Low: 0.28 ± 0.13, Suburban Low: 0.20 ± 0.13), intermediate in the urban medium and high-income neighborhoods (Urban Medium: 0.96 ± 0.12, Urban High: 1.01 ± 0.12), and highest in the suburban medium and high-income neighborhoods (Suburban Medium: 1.81 ± 0.12, Suburban High: 2.24 ± 0.12). Predator abundances were lowest in the urban low-income neighborhood (Urban Low: 0.00 ± 0.16), intermediate in the urban medium and high and suburban low and medium-income neighborhoods (Urban Medium: 0.54 ± 0.26, Urban High: 0.78 ± 0.15, Suburban Low: 1.12 ± 0.14, Suburban Medium: 0.68 ± 0.15), and highest in the suburban high-income neighborhood (Suburban High: 1.94 ± 0.14). 4. Discussion We observed significant differences in arthropod abundances across urban and suburban areas, with greater abundances of both herbivores and predators in high and medium-income suburban areas. Specifically, we found fewer herbivores in low-income areas (urban and suburban), followed by urban medium- and high-income areas, and finally suburban medium- and high-income areas had the highest herbivore abundances. Similarly, the fewest predators were found in urban low-income areas and the most in suburban high-income areas. Altogether, we found that arthropods have higher abundances in suburban locations than in urban ones, indicating that urbanization might decrease arthropod abundance. One might say there are more bugs in the burbs. Our findings indicate that natural forested areas experience significantly greater average herbivorous insect damage than suburban and urban locations, with more zero-damage leaves in urban > suburban > forest. This is consistent with recent research (Bode & Gilbert, 2015 ; Herrmann et al., 2012 ; Kozlov et al., 2017 ; Moreira et al., 2019 ; Schueller et al., 2019 ), which has found decreased insect herbivory with increasing urbanization, thus contributing to a growing body of literature that contradicts past findings that herbivory increases with urbanization (Cuevas-Reyes et al., 2013 ; Dreistadt et al., 1990 ; Raupp et al., 2010 ). Additionally, our study adds a layer of complexity by investigating the impacts of average neighborhood income on leaf damage and arthropod abundances, complicating the urbanization gradient. While we found more zero-damage leaves in medium and high-income urban areas, when excluding zero-damage leaves, we surprisingly found higher average damage on different ends of the income spectrum: suburban high-income (Travilah) and urban low-income areas (Anacostia) had leaves with the greatest herbivore damage. Our arthropod abundance findings contradict the literature, which cites herbivore abundance increasing as urbanization increases, typically attributed to human-caused characteristics of urbanized areas, such as higher temperatures (Just et al., 2019 ; Raupp et al., 2010 ; Youngsteadt et al., 2015 ). However, this is not the case in our study, as we found lower levels of herbivores in urban areas. This disparity may partly be explained by differences across income levels in our study. We found that low-income areas (Anacostia and White Oak) had the lowest herbivore abundances, followed by middle and high-income sites in Washington DC and middle and high-income suburban sites within Montgomery County, Maryland. Predator abundances showed a relatively similar trend to herbivores, with high-income suburban areas having the highest abundance, while the low-income urban area, Anacostia, had significantly lower predator abundance. A factor that could impact herbivore abundance is the difference in habitat availability between urban and suburban locations. On average, urban areas in the DC metropolitan area have less tree coverage and green space than suburban areas, with the suburbs having almost two times the tree coverage compared to the urban areas (Table 1 ). Decreased habitat availability can lead to overcrowding of arthropods on individual trees. Similarly, habitat fragmentation and physical barriers (buildings) may make it difficult for many arthropod species to migrate among trees (Fenoglio et al., 2021 ). This can result in increased competition between urban-dwelling arthropods as fewer habitats are present and accessible. In contrast, a higher number and density of trees in the suburbs could increase arthropod survival and abundance. Additionally, streets and sidewalks confine urban street trees into small regulated grids of soil that reduce nutrient and water uptake by limiting space and increasing soil compaction (Dale & Frank, 2014b ). This nutrient and water stress impacts street trees (Berrang et al., 1985 ) and in turn may impact the herbivorous insects feeding on them. For example, armored-scale insect survival and abundance declines with increasing water stress on street trees (Cockfield & Potter, 1986 ; Hanks & Denno, 1993 ). In addition, impervious surface cover can impact arthropod abundance, with differential impacts based on guild. Penone et al. ( 2013 ) found that mobile Orthopterans were more sensitive to increased impervious surface cover compared to sedentary species. The difference in herbivore abundance in our study compared to the previous literature might be due to these characteristics (ISC and tree cover), as suburban environments tend to be more similar to natural areas and thus may lend themselves to higher arthropod abundance than urban areas. Our results showed that herbivory levels decreased as urbanization increased, which is contradictory to past consensus (Cuevas-Reyes et al., 2013 ; Dreistadt et al., 1990 ; Raupp et al., 2010 ), but is in line with a growing body of recent research finding herbivory to decrease with urbanization (Bode & Gilbert, 2015 ; Herrmann et al., 2012 ; Kozlov et al., 2017 ; Moreira et al., 2019 ; Schueller et al., 2019 ). Because we found similar patterns of herbivore and predator abundances within urban and suburban area types, there is a low likelihood that the level of damage can be attributed to top-down controls ( i.e. , predator abundance controlling herbivore abundance). Instead, the low levels of herbivory in urban areas in our study might be attributed to bottom-up controlling factors common to urban environments. Irrigation and pruning result in foliage with increased nitrogen and decreased secondary defense compounds (Raupp et al., 2010 ), while increased carbon dioxide and nitrogen levels are associated with lower defense levels (Moreira et al., 2019 ). Fossil fuel pollution from transportation, runoff due to high impervious surface coverage ( e.g. , Brightwood and Georgetown with around 60% impervious surface cover) or direct fertilizer application all lead to increased nitrogen content of plants, increasing leaf nutrient quality. Counterintuitively, this increased leaf quality in urban areas may lead to lower levels of herbivory, as herbivores can each consume less per capita and still fulfill their nutritional needs (Kozlov et al., 2017 ; La Pierre & Smith, 2016 ). While the low-income urban area of Anacostia did not follow the same pattern as the other urban sites (decreased herbivory in urban areas), our results do support our prediction that low-income areas would experience higher levels of herbivory. Interestingly, we found the same level of herbivory in low-income Anacostia as in Travilah, the suburban neighborhood with the highest average median household income in our study. This interesting pattern of highest herbivory in the high-income suburbs (Travilah) and low-income urban area (Anacostia) may be related to variations in tree coverage and the uniqueness of DC as an urban city. With the highest tree coverage (63%) and lowest impervious surface coverage (7%; Table 1 ), Travilah has environmental conditions that are more similar to natural forested trees, especially considering that wooded areas surround the neighborhood. High herbivore rates may stem from a “spillover effect” of herbivorous insects from nearby natural forested areas. With growing habitat fragmentation and increased agricultural land use, many studies are investigating the impacts of spillover from natural to managed and managed to natural ecosystems related to herbivores and pests (Blitzer et al., 2012 ) or pathogens such as Ebola and the coronavirus (Alexander et al., 2018 ). To this point, Georgetown, which has considerably lower tree coverage and higher impervious surface coverage than Travilah (Table 1 ), looks and feels like a typical cityscape, with the neighborhood featuring a variety of high-end stores and restaurants. As such, for Georgetown higher income does not equate to more tree coverage. In contrast, while Anacostia residents have the lowest average median household income, they live with higher tree coverage and less impervious surface coverage than Georgetown (Table 1 ). Additionally, Anacostia, similarly to Travilah, has multiple parks within and adjacent to the neighborhood. This green space could explain the similarity between rates of herbivory in Anacostia and Travilah, as the same mechanisms of similarity to forested areas and spillover could be responsible. The health of urban street trees is significant in the context of urban warming, increased pollution, and decreased rainfall, all of which couple with variations in herbivory to impact the ecosystem services street trees provide humans. Street trees play important roles in urban and suburban areas. Urbanization results in more buildings and paved roads, contributing to the urban island heat effect (Arnfield, 2003 ; Freedman, 1995 ; Oke & Maxwell, 1975 ; Price, 1979 ) and increased runoff of pollutants (Haughton & Hunter, 2004 ). Vegetated areas with plants and street trees help lower temperatures (Armson et al., 2012 ), absorb runoff (Bolund & Hunhammar, 1999 ), and reduce the energy usage of surrounding houses and neighborhoods (Huang et al., 2011 ). Considering all the benefits urban street trees provide residents, especially those in low-income neighborhoods, it is important to understand the ecology of street trees in suburban and urban ecosystems. Our results demonstrate the important role of urbanization, income level, and factors such as impervious surface and tree canopy coverage in structuring plant-herbivorous insect interactions, which can help inform street tree management in the future (Dale & Frank, 2017 ). Declarations Acknowledgements Funding was provided by the National Science Foundation Grant #NSF DBI 1950656 to A. Cawood and J. Parker for SERC's Research Experience for Undergraduates program for E. Blake’s REU experience to conduct this research. Author Contributions All authors contributed to the study conception and design. EB, SB, and AH conducted the field research. EB, AH, and KK conducted the statistical analyses. EB wrote the first manuscript draft, with revisions from all authors. All authors have read and approved the final manuscript. Competing Interests Statement: The authors have no relevant financial or non-financial interests to disclose. References Alexander, K. A., Carlson, C. J., Lewis, B. L., Getz, W. M., Marathe, M. V., Eubank, S. G., Sanderson, C. E., & Blackburn, J. K. (2018). The Ecology of Pathogen Spillover and Disease Emergence at the Human-Wildlife-Environment Interface. In C. J. Hurst (Ed.), The Connections Between Ecology and Infectious Disease (pp. 267-298). Springer International Publishing. https://doi.org/10.1007/978-3-319-92373-4_8 Alvey, A. A. (2006). Promoting and preserving biodiversity in the urban forest. Urban Forestry & Urban Greening , 5 (4), 195-201. https://doi.org/10.1016/j.ufug.2006.09.003 Armson, D., Stringer, P., & Ennos, A. R. (2012). The effect of tree shade and grass on surface and globe temperatures in an urban area. Urban Forestry & Urban Greening , 11 (3), 245-255. https://doi.org/https://doi.org/10.1016/j.ufug.2012.05.002 Arnfield, A. J. (2003). Two decades of urban climate research: a review of turbulence, exchanges of energy and water, and the urban heat island. International Journal of Climatology , 23 (1), 1-26. https://doi.org/https://doi.org/10.1002/joc.859 Bagchi, R., Gallery, R. E., Gripenberg, S., Gurr, S. J., Narayan, L., Addis, C. E., Freckleton, R. P., & Lewis, O. T. (2014). Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature , 506 (7486), 85-88. https://doi.org/10.1038/nature12911 Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software , 67 (1), 1 - 48. https://doi.org/10.18637/jss.v067.i01 Beecham, S., & Lucke, T. (2015). Street Trees in Paved Urban Environments: The Benefits and Challenges. Proceeding of the 16th National Street Tree Symposium, Berrang, P., Karnosky, D. F., & Stanton, B. J. (1985). Environmental Factors Affecting Tree Health in New York City. Arboriculture & Urban Forestry (AUF) , 11 (6), 185-189. https://doi.org/10.48044/jauf.1985.042 Bigger, D. S., & Marvier, M. A. (1998). How different would a world without herbivory be?: A search for generality in ecology. Integrative Biology: Issues, News, and Reviews , 1 (2), 60-67. https://doi.org/10.1002/(sici)1520-6602(1998)1:23.0.co;2-z Björkman, C., Dalin, P., & Ahrné, K. (2008). Leaf trichome responses to herbivory in willows: induction, relaxation and costs. New Phytologist , 179 (1), 176-184. https://doi.org/10.1111/j.1469-8137.2008.02442.x Blitzer, E. J., Dormann, C. F., Holzschuh, A., Klein, A.-M., Rand, T. A., & Tscharntke, T. (2012). Spillover of functionally important organisms between managed and natural habitats. Agriculture, Ecosystems & Environment , 146 (1), 34-43. https://doi.org/https://doi.org/10.1016/j.agee.2011.09.005 Bode, R. F., & Gilbert, A. B. (2015). Seed Predators, not Herbivores, Exert Natural Selection on Solidago spp . in an Urban Archipelago. Environmental Entomology , 45 (1), 150-154. https://doi.org/10.1093/ee/nvv158 Bolund, P., & Hunhammar, S. (1999). Ecosystem services in urban areas. Ecological Economics , 29 (2), 293-301. https://doi.org/https://doi.org/10.1016/S0921-8009(99)00013-0 Brooks, M. E., Kristensen, K., Van Benthem, K. J., Magnusson, A., Berg, C. W., Nielsen, A., Skaug, H. J., Machler, M., & Bolker, B. M. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R journal , 9 (2), 378-400. Cabrera, H. M., Argandoña, V. H., & Corcuera, L. J. (1994). Metabolic changes in barley seedlings at different aphid infestation levels. Phytochemistry , 35 (2), 317-319. https://doi.org/10.1016/s0031-9422(00)94755-1 Chakraborty, T., Hsu, A., Manya, D., & Sheriff, G. (2019). Disproportionately higher exposure to urban heat in lower-income neighborhoods: a multi-city perspective. Environmental Research Letters , 14 (10), 105003. https://doi.org/10.1088/1748-9326/ab3b99 Chaves, M. M., Flexas, J., & Pinheiro, C. (2009). Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany , 103 (4), 551-560. https://doi.org/10.1093/aob/mcn125 Cockfield, S. D., & Potter, D. A. (1986). Interaction of Euonymus scale (Homoptera: Diaspididae) feeding damage and severe water stress on leaf abscission and growth of Euonymus fortunei. Oecologia , 71 (1), 41-46. https://doi.org/10.1007/BF00377318 Crawley, M. J. (1989). Insect Herbivores and Plant Population Dynamics. Annual Review of Entomology , 34 (1), 531-562. https://doi.org/10.1146/annurev.en.34.010189.002531 Cuevas-Reyes, P., Gilberti, L., González-Rodríguez, A., & Fernandes, G. W. (2013). Patterns of herbivory and fluctuating asymmetry in Solanum lycocarpum St. Hill (Solanaceae) along an urban gradient in Brazil. Ecological Indicators , 24 , 557-561. https://doi.org/https://doi.org/10.1016/j.ecolind.2012.08.011 Dale, A. G., & Frank, S. D. (2014a). Urban warming trumps natural enemy regulation of herbivorous pests. Ecological Applications , 24 (7), 1596-1607. https://doi.org/https://doi.org/10.1890/13-1961.1 Dale, A. G., & Frank, S. D. (2014b). The Effects of Urban Warming on Herbivore Abundance and Street Tree Condition. PLOS ONE , 9 (7), e102996. https://doi.org/10.1371/journal.pone.0102996 Dale, A. G., & Frank, S. D. (2017). Warming and drought combine to increase pest insect fitness on urban trees. PLOS ONE , 12 (3), e0173844. https://doi.org/10.1371/journal.pone.0173844 Donovan, G. H., & Butry, D. T. (2010). Trees in the city: Valuing street trees in Portland, Oregon. Landscape and Urban Planning , 94 (2), 77-83. https://doi.org/10.1016/j.landurbplan.2009.07.019 Dreistadt, S. H., Dahlsten, D. L., & Frankie, G. W. (1990). Urban Forests and Insect Ecology. BioScience , 40 (3), 192-198. https://doi.org/10.2307/1311364 Felson, A. J., Bradford, M. A., & Terway, T. M. (2013). Promoting Earth Stewardship through urban design experiments. Frontiers in Ecology and the Environment , 11 (7), 362-367. https://doi.org/10.1890/130061 Fenoglio, M. S., Calviño, A., González, E., Salvo, A., & Videla, M. (2021). Urbanisation drivers and underlying mechanisms of terrestrial insect diversity loss in cities. Ecological Entomology , 46 (4), 757-771. https://doi.org/https://doi.org/10.1111/een.13041 Freedman, B. (1995). 1 - THE ECOLOGICAL EFFECTS OF POLLUTION, DISTURBANCE, AND OTHER STRESSES. In B. Freedman (Ed.), Environmental Ecology (Second Edition) (pp. 1-10). Academic Press. https://doi.org/https://doi.org/10.1016/B978-0-08-050577-0.50006-6 Getman-Pickering, Z. L., Campbell, A., Aflitto, N., Grele, A., Davis, J. K., & Ugine, T. A. (2020). LeafByte: A mobile application that measures leaf area and herbivory quickly and accurately. Methods in Ecology and Evolution , 11 (2), 215-221. https://doi.org/https://doi.org/10.1111/2041-210X.13340 Hanks, L. M., & Denno, R. F. (1993). Natural Enemies and Plant Water Relations Influence the Distribution of an Armored Scale Insect. Ecology , 74 (4), 1081-1091. https://doi.org/https://doi.org/10.2307/1940478 Haughton, G., & Hunter, C. (2004). Sustainable cities . Routledge. Herrmann, D. L., Pearse, I. S., & Baty, J. H. (2012). Drivers of specialist herbivore diversity across 10 cities. Landscape and Urban Planning , 108 (2), 123-130. https://doi.org/https://doi.org/10.1016/j.landurbplan.2012.08.007 Hilbert, D., Roman, L., Koeser, A., Vogt, J., & Van Doorn, N. (2018). Urban Tree Mortality: A Literature Review . https://doi.org/10.13140/RG.2.2.25953.15204 Hoffman, J. S., Shandas, V., & Pendleton, N. (2020). The effects of historical housing policies on resident exposure to intra-urban heat: a study of 108 US urban areas. Climate , 8 (1), 12. Hsu, A., Sheriff, G., Chakraborty, T., & Manya, D. (2021). Disproportionate exposure to urban heat island intensity across major US cities. Nature Communications , 12 (1), 2721. https://doi.org/10.1038/s41467-021-22799-5 Huang, G., Zhou, W., & Cadenasso, M. L. (2011). Is everyone hot in the city? Spatial pattern of land surface temperatures, land cover and neighborhood socioeconomic characteristics in Baltimore, MD. Journal of Environmental Management , 92 (7), 1753-1759. https://doi.org/https://doi.org/10.1016/j.jenvman.2011.02.006 Johnson, S. N., Erb, M., & Hartley, S. E. (2016). Roots under attack: contrasting plant responses to below‐ and aboveground insect herbivory. New Phytologist , 210 (2), 413-418. https://doi.org/10.1111/nph.13807 Just, M. G., Dale, A. G., Long, L. C., & Frank, S. D. (2019). Urbanization drives unique latitudinal patterns of insect herbivory and tree condition. Oikos , 128 (7), 984-993. https://doi.org/https://doi.org/10.1111/oik.05874 Kaakeh, W., Pfeiffer, D. G., & Marini, R. P. (1992). Combined Effects of Spirea Aphid (Homoptera: Aphididae) and Nitrogen Fertilization on Net Photosynthesis, Total Chlorophyll Content, and Greenness of Apple Leaves. Journal of Economic Entomology , 85 (3), 939-946. https://doi.org/10.1093/jee/85.3.939 Kozlov, M. V., Lanta, V., x11b, ch, Zverev, V. E., & Zvereva, E. L. (2012). Delayed local responses of downy birch to damage by leafminers and leafrollers. Oikos , 121 (3), 428-434. http://www.jstor.org/stable/41428987 Kozlov, M. V., Lanta, V., Zverev, V., Rainio, K., Kunavin, M. A., & Zvereva, E. L. (2017). Decreased losses of woody plant foliage to insects in large urban areas are explained by bird predation. Global Change Biology , 23 (10), 4354-4364. https://doi.org/https://doi.org/10.1111/gcb.13692 Kozlov, M. V., Lanta, V., Zverev, V., & Zvereva, E. L. (2015). Global patterns in background losses of woody plant foliage to insects. Global Ecology and Biogeography , 24 (10), 1126-1135. https://doi.org/10.1111/geb.12347 Kozlov, M. V., Zverev, V., & Zvereva, E. L. (2014). Confirmation bias leads to overestimation of losses of woody plant foliage to insect herbivores in tropical regions. PeerJ , 2 , e709. https://doi.org/10.7717/peerj.709 Kozlov, M. V., & Zvereva, E. L. (2018). Background Insect Herbivory: Impacts, Patterns and Methodology. In F. M. Cánovas, U. Lüttge, & R. Matyssek (Eds.), Progress in Botany Vol. 79 (pp. 313-355). Springer International Publishing. https://doi.org/10.1007/124_2017_4 La Pierre, K. J., & Smith, M. D. (2016). Soil nutrient additions increase invertebrate herbivore abundances, but not herbivory, across three grassland systems. Oecologia , 180 (2), 485-497. https://doi.org/10.1007/s00442-015-3471-7 Lahr, E. C., Dunn, R. R., & Frank, S. D. (2018). Variation in photosynthesis and stomatal conductance among red maple (Acer rubrum) urban planted cultivars and wildtype trees in the southeastern United States. PLOS ONE , 13 (5), e0197866. https://doi.org/10.1371/journal.pone.0197866 Lamarre, G. P. A., Baraloto, C., Fortunel, C., Dávila, N., Mesones, I., Rios, J. G., Ríos, M., Valderrama, E., Pilco, M. V., & Fine, P. V. A. (2012). Herbivory, growth rates, and habitat specialization in tropical tree lineages: implications for Amazonian beta-diversity. Ecology , 93 (8), S195-S210. http://www.jstor.org/stable/23229916 Landry, S. M., & Chakraborty, J. (2009). Street Trees and Equity: Evaluating the Spatial Distribution of an Urban Amenity. Environment and Planning A: Economy and Space , 41 (11), 2651-2670. https://doi.org/10.1068/a41236 Marquis, R. J., & Whelan, C. J. (1994). Insectivorous Birds Increase Growth of White Oak through Consumption of Leaf-Chewing Insects. Ecology , 75 (7), 2007-2014. https://doi.org/10.2307/1941605 Metcalfe, D. B., Asner, G. P., Martin, R. E., Silva Espejo, J. E., Huasco, W. H., Farfán Amézquita, F. F., Carranza‐Jimenez, L., Galiano Cabrera, D. F., Baca, L. D., Sinca, F., Huaraca Quispe, L. P., Taype, I. A., Mora, L. E., Dávila, A. R., Solórzano, M. M., Puma Vilca, B. L., Laupa Román, J. M., Guerra Bustios, P. C., Revilla, N. S., . . . Malhi, Y. (2014). Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecology Letters , 17 (3), 324-332. https://doi.org/10.1111/ele.12233 Moreira, X., Abdala-Roberts, L., Berny Mier y Teran, J. C., Covelo, F., de la Mata, R., Francisco, M., Hardwick, B., Pires, R. M., Roslin, T., Schigel, D. S., ten Hoopen, J. P. J. G., Timmermans, B. G. H., van Dijk, L. J. A., Castagneyrol, B., & Tack, A. J. M. (2019). Impacts of urbanization on insect herbivory and plant defences in oak trees. Oikos , 128 (1), 113-123. https://doi.org/https://doi.org/10.1111/oik.05497 Mullaney, J., Lucke, T., & Trueman, S. J. (2015). A review of benefits and challenges in growing street trees in paved urban environments. Landscape and Urban Planning , 134 , 157-166. https://doi.org/10.1016/j.landurbplan.2014.10.013 Nabity, P. D., Zavala, J. A., & Delucia, E. H. (2009). Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Annals of Botany , 103 (4), 655-663. https://doi.org/10.1093/aob/mcn127 National Wildlife Federation. Red Maple . https://www.nwf.org/Home/Educational-Resources/Wildlife-Guide/Plants-and-Fungi/Red-Maple Oke, T. R., & Maxwell, G. B. (1975). Urban heat island dynamics in Montreal and Vancouver. Atmospheric Environment (1967) , 9 (2), 191-200. https://doi.org/https://doi.org/10.1016/0004-6981(75)90067-0 Pataki, D. E., Alberti, M., Cadenasso, M. L., Felson, A. J., McDonnell, M. J., Pincetl, S., Pouyat, R. V., Setälä, H., & Whitlow, T. H. (2021). The Benefits and Limits of Urban Tree Planting for Environmental and Human Health. Frontiers in Ecology and Evolution , 9 . https://doi.org/10.3389/fevo.2021.603757 Penone, C., Kerbiriou, C., Julien, J.-F., Julliard, R., Machon, N., & Le Viol, I. (2013). Urbanisation effect on Orthoptera: which scale matters? Insect Conservation and Diversity , 6 (3), 319-327. https://doi.org/https://doi.org/10.1111/j.1752-4598.2012.00217.x Price, J. C. (1979). Assessment of the Urban Heat Island Effect Through the Use of Satellite Data. Monthly Weather Review , 107 (11), 1554-1557. https://doi.org/https://doi.org/10.1175/1520-0493(1979)1072.0.CO;2 Raupp, M. J., Shrewsbury, P. M., & Herms, D. A. (2010). Ecology of Herbivorous Arthropods in Urban Landscapes. Annual Review of Entomology , 55 (1), 19-38. https://doi.org/10.1146/annurev-ento-112408-085351 Schaffer, B., & Mason, L. J. (1990). Effects of scale insect herbivory and shading on net gas exchange and growth of a subtropical tree species (Guaiacum sanctum L.). Oecologia , 84 (4), 468-473. https://doi.org/10.1007/BF00328162 Schmitt, L., & Burghardt, K. T. (2021). Urbanization as a disrupter and facilitator of insect herbivore behaviors and life cycles. Current Opinion in Insect Science , 45 , 97-105. https://doi.org/https://doi.org/10.1016/j.cois.2021.02.016 Schueller, S. K., Paul, S., Payer, N., Schultze, R., & Vikas, M. (2019). Urbanization decreases the extent and variety of leaf herbivory for native canopy tree species Quercus rubra, Quercus alba, and Acer saccharum. Urban Ecosystems , 22 (5), 907-916. https://doi.org/10.1007/s11252-019-00866-6 Soares, A. L., Rego, F. C., McPherson, E. G., Simpson, J. R., Peper, P. J., & Xiao, Q. (2011). Benefits and costs of street trees in Lisbon, Portugal. Urban Forestry & Urban Greening , 10 (2), 69-78. https://doi.org/10.1016/j.ufug.2010.12.001 The Herbivory Variability Network, Robinson, M. L., Hahn, P. G., Inouye, B. D., Underwood, N., Whitehead, S. R., Abbott, K. C., Bruna, E. M., Cacho, N. I., Dyer, L. A., Abdala-Roberts, L., Allen, W. J., Andrade, J. F., Angulo, D. F., Anjos, D., Anstett, D. N., Bagchi, R., Bagchi, S., Barbosa, M., . . . Wetzel, W. C. (2023). Plant size, latitude, and phylogeny explain within-population variability in herbivory. Science , 382 (6671), 679-683. https://doi.org/doi:10.1126/science.adh8830 Turner‐Skoff, J. B., & Cavender, N. (2019). The benefits of trees for livable and sustainable communities. PLANTS, PEOPLE, PLANET , 1 (4), 323-335. https://doi.org/10.1002/ppp3.39 Turrini, T., Sanders, D., & Knop, E. (2016). Effects of urbanization on direct and indirect interactions in a tri‐trophic system. Ecological Applications , 26 (3), 664-675. https://doi.org/10.1890/14-1787 Walters, R. S., & Yawney, H. W. (1990). Acer rubrum L. Red maple. Silvics of North America , 2 , 60-69. Welter, S. C. (1989). Arthropod Impact on Plant Gas Exchange. In (pp. 135-164). CRC Press. https://doi.org/10.1201/9780429290916-5 Wolf, K. L., Lam, S. T., McKeen, J. K., Richardson, G. R. A., van den Bosch, M., & Bardekjian, A. C. (2020). Urban Trees and Human Health: A Scoping Review. International Journal of Environmental Research and Public Health , 17 (12), 4371. https://www.mdpi.com/1660-4601/17/12/4371 Young, R. F. (2010). Managing municipal green space for ecosystem services. Urban Forestry & Urban Greening , 9 (4), 313-321. https://doi.org/https://doi.org/10.1016/j.ufug.2010.06.007 Youngsteadt, E., Dale, A. G., Terando, A. J., Dunn, R. R., & Frank, S. D. (2015). Do cities simulate climate change? A comparison of herbivore response to urban and global warming. Global Change Biology , 21 (1), 97-105. https://doi.org/https://doi.org/10.1111/gcb.12692 Zangerl, A. R., Hamilton, J. G., Miller, T. J., Crofts, A. R., Oxborough, K., Berenbaum, M. R., & De Lucia, E. H. (2002). Impact of folivory on photosynthesis is greater than the sum of its holes. Proceedings of the National Academy of Sciences , 99 (2), 1088-1091. https://doi.org/10.1073/pnas.022647099 Zvereva, E. L., Zverev, V., & Kozlov, M. V. (2012). Little strokes fell great oaks: minor but chronic herbivory substantially reduces birch growth. Oikos , 121 (12), 2036-2043. http://www.jstor.org/stable/41686695 Additional Declarations No competing interests reported. Cite Share Download PDF Status: Published Journal Publication published 25 Jul, 2024 Read the published version in Urban Ecosystems → Version 1 posted Editorial decision: Revision requested 08 May, 2024 Reviews received at journal 08 May, 2024 Reviews received at journal 06 May, 2024 Reviewers agreed at journal 21 Apr, 2024 Reviewers agreed at journal 21 Apr, 2024 Reviewers agreed at journal 15 Apr, 2024 Reviewers agreed at journal 13 Apr, 2024 Reviewers invited by journal 13 Apr, 2024 Editor assigned by journal 08 Apr, 2024 Submission checks completed at journal 08 Apr, 2024 First submitted to journal 04 Apr, 2024 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4219885","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":288914662,"identity":"4276a88e-534d-4001-8fc8-74d525b6f0be","order_by":0,"name":"Elizabeth Blake","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAs0lEQVRIiWNgGAWjYFACHsYDDAcY5CBsIrUwgLQYk64lsYFoLfxiZw8c+HHGJn3DjQTGB2/biNAiOTsv4WDPjbRcoBZmw7nEaDG4nWNwgOfD4dwNtxPYpHmJ0WIP1HLwz4f/6Qa3E9h/E6XFQDrH4DDPjQMJQC1szERpkbidl3BY5kyy4cz7D5sl55wjQgv/7NyDD98cs5PnO3P44Ic3ZURoQQKMDaSpHwWjYBSMglGAGwAA9rQ+0oM+F4MAAAAASUVORK5CYII=","orcid":"","institution":"University of Washington School of Public Health","correspondingAuthor":true,"prefix":"","firstName":"Elizabeth","middleName":"","lastName":"Blake","suffix":""},{"id":288914663,"identity":"336e969c-2767-4d7c-96c7-f7e2b637c723","order_by":1,"name":"Shelley Bennett","email":"","orcid":"","institution":"Smithsonian Environmental Research Center","correspondingAuthor":false,"prefix":"","firstName":"Shelley","middleName":"","lastName":"Bennett","suffix":""},{"id":288914664,"identity":"ebfceb4d-7554-461f-a0da-90b60e10aac5","order_by":2,"name":"Amy Hruska","email":"","orcid":"","institution":"Underwood and Associates","correspondingAuthor":false,"prefix":"","firstName":"Amy","middleName":"","lastName":"Hruska","suffix":""},{"id":288914665,"identity":"59a8c9d6-4824-4d04-b694-28122c58168d","order_by":3,"name":"Kimberly J Komatsu","email":"","orcid":"","institution":"University of North Carolina at Greensboro","correspondingAuthor":false,"prefix":"","firstName":"Kimberly","middleName":"J","lastName":"Komatsu","suffix":""}],"badges":[],"createdAt":"2024-04-04 22:00:20","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4219885/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4219885/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1007/s11252-024-01584-4","type":"published","date":"2024-07-26T00:36:44+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":54522746,"identity":"320c2b95-8772-4c9f-8540-82d26c337438","added_by":"auto","created_at":"2024-04-11 18:34:14","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":1019307,"visible":true,"origin":"","legend":"\u003cp\u003eMap of the greater Washington, DC area with neighborhood study sites colored based to income level (yellow, low; medium, teal; high, navy blue). Urban sites were all within the Washington, DC boundaries, depicted by the black square line. Suburban sites were in the surrounding area and the natural forested location in Edgewater, Maryland is depicted with a star.\u003c/p\u003e","description":"","filename":"floatimage1.png","url":"https://assets-eu.researchsquare.com/files/rs-4219885/v1/02f6f3c7c05863c8faf0052d.png"},{"id":54522745,"identity":"f05330c1-104f-4b95-abb7-3adab723c5bb","added_by":"auto","created_at":"2024-04-11 18:34:14","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":18993,"visible":true,"origin":"","legend":"\u003cp\u003eDistribution of leaf damage values observed across land use types. Lowercase letters along the bottoms of the distributions represent significant differences in the probability of occurrence of zero leaf damage among neighborhoods, while uppercase letters along the top represent significant differences in the mean percent damage of leaves where damage was observed.\u003c/p\u003e","description":"","filename":"floatimage3.png","url":"https://assets-eu.researchsquare.com/files/rs-4219885/v1/2d3da5040efc2163378e96c6.png"},{"id":54522747,"identity":"646f899f-4dc2-47cd-9cd6-48ca2c00a4dc","added_by":"auto","created_at":"2024-04-11 18:34:14","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":261766,"visible":true,"origin":"","legend":"\u003cp\u003eDistribution of leaf damage values observed across land use types stratified by neighborhood income level. Lowercase letters along the bottoms of the distributions represent significant differences in the probability of occurrence of zero leaf damage among neighborhoods, while uppercase letters along the tops represent significant differences in the mean percent damage of leaves where damage was observed.\u003c/p\u003e","description":"","filename":"floatimage4.png","url":"https://assets-eu.researchsquare.com/files/rs-4219885/v1/57e5e3c689995a3c22c80aeb.png"},{"id":54522748,"identity":"4cf13a02-9ef5-43c1-bb7f-faa49d530613","added_by":"auto","created_at":"2024-04-11 18:34:14","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":29152,"visible":true,"origin":"","legend":"\u003cp\u003eDistribution of (left) herbivore and (right) predator abundance values observed across land use types stratified by neighborhood income level. Lowercase letters represent significant differences in the herbivore and predator abundances across neighborhoods.\u003c/p\u003e","description":"","filename":"floatimage5.png","url":"https://assets-eu.researchsquare.com/files/rs-4219885/v1/e18a20cfece88585a4f70487.png"},{"id":61198040,"identity":"fff7ca24-20b6-42c4-9259-39b2d3b04670","added_by":"auto","created_at":"2024-07-27 00:36:47","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":3894,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4219885/v1/c76dc55c-8d06-49cb-a3a2-bdf78c8f6558.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Insect herbivory on Acer rubrum varies across income and urbanization gradients in the D.C. metropolitan area","fulltext":[{"header":"1. Introduction","content":"\u003cp\u003eTrees are key components of many urban ecosystems. In particular, street trees are important for cities as they supply environmental, economic, and social benefits for their city\u0026rsquo;s residents (Donovan \u0026amp; Butry, \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Landry \u0026amp; Chakraborty, \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Mullaney et al., \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Soares et al., \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Wolf et al., \u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Thus, urban planning must critically consider tree health (Alvey, \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Felson et al., \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). While tree health is impacted by abiotic and biotic factors (Hilbert et al., \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2018\u003c/span\u003e), herbivory in particular can have large consequences for tree growth, success, and survival (Crawley, \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e1989\u003c/span\u003e). Further, herbivory can impact ecosystem productivity by modifying nutrient cycling (Bagchi et al., \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Lamarre et al., \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Metcalfe et al., \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2014\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eUrban street trees provide invaluable ecosystem services to their surrounding environment (Beecham \u0026amp; Lucke, \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Turner-Skoff \u0026amp; Cavender, \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). For example, urban trees can serve as habitats for various species, increasing species diversity in urban ecosystems (Pataki et al., \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). This being considered, it is important to understand how trees and their herbivorous residents are impacted by increasing urbanization (Lahr et al., \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2018\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eOn average, plants suffer greater effects from invertebrates than from vertebrate herbivores (Bigger \u0026amp; Marvier, \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e1998\u003c/span\u003e). While most damage from an individual herbivorous insect may be minor, collectively they can substantially damage plants, even at low densities (Kozlov \u0026amp; Zvereva, \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Herbivory results in tissue removal, which decreases leaf area and directly impacts photosynthesis, growth, leaf abscission, costly induced defenses, and leaf vulnerability to pathogens (Bj\u0026ouml;rkman et al., \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2008\u003c/span\u003e; Kozlov et al., \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Kozlov et al., \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Marquis \u0026amp; Whelan, \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e1994\u003c/span\u003e). For example, sap-feeding herbivores can cause a reduction in chlorophyll content and decrease stomatal conductance, limiting photosynthesis and cell respiration (Cabrera et al., \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e1994\u003c/span\u003e; Kaakeh et al., \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e1992\u003c/span\u003e; Nabity et al., \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Schaffer \u0026amp; Mason, \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e1990\u003c/span\u003e). Similarly, root feeders disrupt water and nutrient uptake (Johnson et al., \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2016\u003c/span\u003e), impacting photosynthesis by indirectly decreasing CO\u003csub\u003e2\u003c/sub\u003e availability and altering photosynthetic metabolism and oxidative stress (Chaves et al., \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2009\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eWhile sap and root feeders play a part in plant health, it is estimated that 90% of leaf damage is due to externally feeding defoliators (Kozlov et al., \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Not only does foliar herbivory remove leaf tissue, but leaf damage has the potential to impact surrounding tissue (Nabity et al., \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Welter, \u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e1989\u003c/span\u003e; Zangerl et al., \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2002\u003c/span\u003e), further limiting photosynthetic capabilities. This cycle is further propelled as decreased photosynthesis can lead to reduced bud development and production of smaller leaves, which sets up a positive feedback loop by providing less support to subsequent buds, resulting in shorter shoots the following growing season (Zvereva et al., \u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). Thus, understanding the effects of foliar insect herbivory on urban trees is essential for promoting their health and maintenance.\u003c/p\u003e \u003cp\u003ePrevious research shows conflicting patterns related to herbivore abundance on trees in urban settings. There is little evidence for a universal increase in herbivore abundance or species richness along urbanization gradients, although guild-specific trends have been identified (Raupp et al., \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). Specifically, Coleoptera (beetles) and Lepidoptera (butterflies and moths) tend to decrease in abundance, while Hemipterans (true bugs) often increase in abundance in cities relative to less urban environments (Schmitt \u0026amp; Burghardt, \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). In their review, Raupp et al. (\u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2010\u003c/span\u003e) found that most small arthropods with sucking mouthparts, limited mobility, multiple generations on the same host plant, or other intimate associations with hosts generally increase along an urbanization gradient. Understanding the consequences of these urbanization impacts on herbivore abundances and community composition for plant damage levels is a critical knowledge gap.\u003c/p\u003e \u003cp\u003eExisting studies that compare herbivory rates between urban and rural areas are conflicting, with some demonstrating that urban trees experienced higher levels of insect herbivory relative to rural habitats (Cuevas-Reyes et al., \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Turrini et al., \u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e2016\u003c/span\u003e), while others found decreased herbivory in urban environments (Bode \u0026amp; Gilbert, \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Herrmann et al., \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Kozlov et al., \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Moreira et al., \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Although urbanization's effect on herbivory rates on street trees has been studied across several cities (Moreira et al., \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), no studies have holistically considered how the economic characteristics of urban areas may impact herbivory. While FDR\u0026rsquo;s New Deal attempted to boost the economy during the Great Depression, it ended up having lasting effects on communities\u0026rsquo; racial and socioeconomic makeup; redlining and restricting people of a certain race or class to specific neighborhoods became common (Young, \u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). Formerly redlined neighborhoods are less developed by the city, often lacking infrastructure and green space, which leaves already vulnerable populations exposed to higher temperatures due to the urban island heat effect and a variety of other environmental threats (Chakraborty et al., \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Hoffman et al., \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Hsu et al., \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Thus, it is not representative to group together all neighboring communities within a city when examining plant-herbivore interactions, as these communities can vary significantly due to the impacts of segregation on the urban landscape\u0026rsquo;s features and characteristics. The lack of nuanced studies considering income gradients in addition to urbanization level may explain the discrepancies we currently see in the literature regarding the role of urbanization on herbivory rates.\u003c/p\u003e \u003cp\u003eRed maple (\u003cem\u003eAcer rubrum\u003c/em\u003e) is native to and ubiquitous across the eastern United States (Walters \u0026amp; Yawney, \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e1990\u003c/span\u003e) and is a popular street tree species planted for its generalist nature and ability to grow in a range of soil conditions (National Wildlife Federation). Despite how abundant and widespread red maple is, few studies have focused specifically on red maple in an urban context. The limited research that exists demonstrated that red maple was negatively impacted by urban warming (Dale \u0026amp; Frank, \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2014a\u003c/span\u003e, \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2014b\u003c/span\u003e) due to increased fecundity, abundance, and survival of the gloomy scale (\u003cem\u003eMelanaspis tenebricosa\u003c/em\u003e) on these trees (Dale \u0026amp; Frank, \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2017\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIn this study, we examine 1800 red maple leaves to determine whether herbivory levels vary along an urbanization gradient and across income levels within urbanization types in the D.C. metropolitan area. We compared herbivorous insect chewing damage on leaves of red maple in the District of Columbia; Montgomery County, Maryland; and the natural forested area of the Smithsonian Environmental Research Center (SERC) in Edgewater, Maryland. We sought to determine whether leaf damage on red maple varies along the urbanization gradient, with the expectation that leaf damage will be positively correlated with urbanization (urban\u0026thinsp;\u0026gt;\u0026thinsp;suburban\u0026thinsp;\u0026gt;\u0026thinsp;forested). We also examined whether income level within urban and suburban areas impacts leaf damage or arthropod abundances. We predicted a negative relationship between arthropods abundance and neighborhood income levels, with arthropod abundance and herbivory being inversely related to income due to increased temperatures and heat stress (low\u0026thinsp;\u0026gt;\u0026thinsp;medium\u0026thinsp;\u0026gt;\u0026thinsp;high income).\u003c/p\u003e"},{"header":"2. Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003e2.1. Study Sites\u003c/h2\u003e \u003cp\u003eThe D.C. Metropolitan area encompasses the District of Columbia (D.C.) and surrounding Maryland and Virginia suburban areas. Here we focus on sites in the District of Columbia, Montgomery County, Maryland and Anne Arundel County, Maryland. Study sites were selected based on red maple presence and categorized based on green space, percent pavement cover, and income. Sites were grouped into urban (District of Columbia), suburban (Montgomery County), and natural forested areas SERC (Anne Arundel County). Within the urban and suburban locations, three neighborhoods were chosen to span median household income levels (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e; Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Census data were used to determine the median household income of the various census block groups of the sites, with classification into high, middle, and low-income were adapted from census-designated income brackets: high-income (\u003cspan\u003e$\u003c/span\u003e121,000 and up), middle-income (\u003cspan\u003e$\u003c/span\u003e84,000 - \u003cspan\u003e$\u003c/span\u003e121,000), and low-income (\u003cspan\u003e$\u003c/span\u003e48,600 - \u003cspan\u003e$\u003c/span\u003e84,000) (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Within D.C. (urban), the Anacostia (low-income), Brightwood (middle-income), and Georgetown (high-income) neighborhoods were included in this study. In Montgomery County (suburban), the White Oak (low-income), Rockville (middle-income), and Travilah (high-income) neighborhoods were sampled in this study. To compare the levels of herbivory observed in the human-dominated areas to a natural forest, three sites within the 2650-acre forested grounds of the Smithsonian Environmental Research Center (Anne Arundel County, Maryland) were also selected for sampling (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eTable of neighborhood characteristics for each of the six human-dominated study sites.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Taba\" border=\"1\"\u003e \u003ccolgroup cols=\"7\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eAnacostia \u003c/p\u003e \u003cp\u003e[Urban, Low-Income]\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eBrightwood\u003c/p\u003e \u003cp\u003e[Urban, Mid-Income]\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eGeorgetown\u003c/p\u003e \u003cp\u003e[Urban, High-Income]\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003eWhite Oak\u003c/p\u003e \u003cp\u003e[Suburban, Low-Income]\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003eRockville\u003c/p\u003e \u003cp\u003e[Suburban, Mid-Income]\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\"\u003e \u003cp\u003eTravilah\u003c/p\u003e \u003cp\u003e[Suburban, High-Income]\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eArea\u003c/p\u003e \u003cp\u003e(sq mi)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e1.1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e5.2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e0.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e10.4\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePopulation Size\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e4,086\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e11,823\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e9,495\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e19,426\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e3,281\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e5,800\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eMedian Household Income\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cspan\u003e$\u003c/span\u003e53,501\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e\u003cspan\u003e$\u003c/span\u003e77,055\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e\u003cspan\u003e$\u003c/span\u003e178,756\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e\u003cspan\u003e$\u003c/span\u003e104,580\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e\u003cspan\u003e$\u003c/span\u003e124,821\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e\u003cspan\u003e$\u003c/span\u003e250,001\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003ePercent Below Poverty Level\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e21.6%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e11.6%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e8.9%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e10.1%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e3.9%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e1.4%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTree Coverage\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e34%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e21%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e30%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e53%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e56%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e63%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eImpervious Surface Coverage\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e50%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e60%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e62%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e27%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e20%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003e7%\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003e2.2 Study Species\u003c/h2\u003e \u003cp\u003eRed maple was chosen as a study species, as it is abundant across land-use types in the study region and the Northeast United States. In July of 2021, we sampled 10 red maple trees at each of our 9 study sites (N\u0026thinsp;=\u0026thinsp;90 trees across all sites). Trees in each area were selected haphazardly, ensuring no directly neighboring trees were sampled. Each tree was roughly divided into four quadrants for sampling the arthropod community (urban and suburban sites) and herbivorous insect foliar damage (all sites).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003e2.3 Arthropod Collection\u003c/h2\u003e \u003cp\u003eWithin the urban and suburban sites, we utilized a 91.44 x 91.44 cm beat sheet to collect arthropods from each of the four quadrants of each sample tree, utilizing a 30 ft pole to beat the branches in the quadrant for 15 seconds (1 minute total per tree). Arthropods that fell from the tree were collected from the beat sheet using an aspirator and placed into labeled collection tubes. Total arthropod abundance per tree was based on the summing of abundances found in each quadrant. Arthropods were not sampled from the natural forest sites due to the inaccessibility of tree branches.\u003c/p\u003e \u003cp\u003eThe arthropods were sorted into herbivores and predators based on broad taxonomic groupings using protocols developed by the Herbivory Variability Network (The Herbivory Variability Network et al., \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Herbivores identified included: grasshoppers/crickets/katydids, caterpillar-like, hoppers, aphids, thrips, mirid, mites, herbivorous beetles, and whiteflies/mealybugs/scale insects. Predators identified included: wasps, spiders, assassins, and predator beetles.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003e2.4 Leaf Collection\u003c/h2\u003e \u003cp\u003eTwenty leaves were randomly selected each of red maple (N\u0026thinsp;=\u0026thinsp;1800 leaves in total), with five leaves collected within each of the four quadrants of each tree. Using a 30-foot extendable pole pruner, leaves were randomly selected from branches at various heights and different distances from the tree\u0026rsquo;s trunk to provide a comprehensive sample of each entire tree. To ensure the leaves suffered no additional damage after collection, all leaves were carefully placed in bags labeled by the site/tree number, placed in a cooler for transport to the lab, and kept refrigerated until processing.\u003c/p\u003e \u003cp\u003ePhotos of all leaves were taken within a week of collection and uploaded into the LeafByte application (Getman-Pickering et al., \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2020\u003c/span\u003e), which we used to estimate percent leaf damage due to herbivory. In some cases, when large sections of the leaf were missing, we made an educated guess of the original outlines of the leaf, and the percent missing was then calculated with this supplemented information. In addition, great care was taken to ensure only herbivory was considered. Instances of tissue loss due to fungal infection, tearing, wind, or sun damage were excluded from the total percentage using the exclude feature in the LeafByte application. Percent damage was recorded for all leaves in the sample set.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003e2.5. Statistical Analysis\u003c/h2\u003e \u003cp\u003eAll statistics were completed in R version 4.1.3. Leaf damage data were continuous and highly zero-inflated. As such, we conducted two-stage mixed-effects models using the \u003cem\u003elme4\u003c/em\u003e package (Bates et al., \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2015\u003c/span\u003e) to examine the effects of (a) land use type, including all data from forest, suburban, and urban sites, and (b) interactive effects of land use and income for the suburban and urban sites only. These two-stage models consisted of first examining the probability of observing zero values for percent leaf damage using logistic regression with a binomial distribution and including land use or land use by income interactions, as appropriate, as fixed factors and tree identity as a random effect. Then we examined the non-zero continuous data using a second model with log-transformed percent leaf damage as the dependent variable, land use or land use by income interactions, as appropriate, as fixed factors, and tree identity as a random effect.\u003c/p\u003e \u003cp\u003eHerbivore and predator count data were analyzed for the suburban and urban sites only using the \u003cem\u003eglmmTMB\u003c/em\u003e package (Brooks et al., \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2017\u003c/span\u003e), including land use by income interactions as fixed factors, tree identity as a random effect, and using a single zero-inflation parameter and a negative binomial distribution.\u003c/p\u003e \u003c/div\u003e"},{"header":"3. Results","content":"\u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003e3.1 Leaf Damage by Area Type and Income\u003c/h2\u003e \u003cp\u003eRoughly 35% (635 of 1800 leaves) of leaves sampled experienced zero damage. Land use significantly affected the incidence of leaf herbivory, with a significantly higher probability of zero damage on urban leaves than suburban leaves and the lowest probability of zero damage on forest leaves (Fig.\u0026nbsp;2; x\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;227.24, df\u0026thinsp;=\u0026thinsp;2, p\u0026thinsp;\u0026lt;\u0026thinsp;0.001). Of the leaves with any damage, most damage values were low, with 45% (526 leaves) of damaged leaves having less than 1% damage and an additional 53% (614 leaves) of damaged leaves having between 1\u0026ndash;20% damage. When considering leaves with damage, urban and suburban leaves had significantly lower average percent damage than forest leaves (Fig.\u0026nbsp;2; x\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;8.07, df\u0026thinsp;=\u0026thinsp;2, p\u0026thinsp;=\u0026thinsp;0.018; means\u0026thinsp;\u0026plusmn;\u0026thinsp;standard errors were as follows, Urban: 0.89% \u0026plusmn; 0.12%, Suburban: 0.93% \u0026plusmn; 0.09%, Forest: 1.23% \u0026plusmn; 0.12%). Despite these average trends, urban and suburban leaves were more likely to experience very high levels of leaf damage (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e; 8 urban leaves and 13 suburban leaves experienced greater than 20% damage, compared to only 4 forest leaves with such high damage values).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eWhen considering only the urban and suburban sites, income significantly interacted with land use to impact percent leaf damage (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). Specifically, a significantly higher probability of zero damage was observed for urban leaves in medium and high-income neighborhoods than low-income urban neighborhoods, and low and high-income suburban neighborhoods were less likely to have zero damage leaves than urban neighborhoods of any income level (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e; x\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;10.66, df\u0026thinsp;=\u0026thinsp;2, p\u0026thinsp;=\u0026thinsp;0.005). When considering leaves with damage, leaves from high-income suburban and low-income urban neighborhoods had significantly greater damage than leaves from all other neighborhoods (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e; x\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;37.41, df\u0026thinsp;=\u0026thinsp;2, p\u0026thinsp;\u0026lt;\u0026thinsp;0.001; means\u0026thinsp;\u0026plusmn;\u0026thinsp;standard errors were as follows, Suburban Low: 0.78% \u0026plusmn; 0.13%, Suburban Medium: 0.59% \u0026plusmn; 0.10%, Suburban High: 1.56% \u0026plusmn; 0.25%, Urban Low: 1.83% \u0026plusmn; 0.35%, Urban Medium: 0.70% \u0026plusmn; 0.16%, Urban High: 0.54% \u0026plusmn; 0.13%).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec10\" class=\"Section2\"\u003e \u003ch2\u003e3.2 Arthropods Abundance by Area Type and Income\u003c/h2\u003e \u003cp\u003eAcross the urban and suburban sites, there was a significant interactive effect of land use and neighborhood income on invertebrate herbivore (x\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;148.50, df\u0026thinsp;=\u0026thinsp;2, p\u0026thinsp;\u0026lt;\u0026thinsp;0.001) and predator abundances (x\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;124.69, df\u0026thinsp;=\u0026thinsp;2, p\u0026thinsp;\u0026lt;\u0026thinsp;0.001). Specifically, herbivore abundances were lowest in the urban and suburban low-income neighborhoods (Urban Low: 0.28\u0026thinsp;\u0026plusmn;\u0026thinsp;0.13, Suburban Low: 0.20\u0026thinsp;\u0026plusmn;\u0026thinsp;0.13), intermediate in the urban medium and high-income neighborhoods (Urban Medium: 0.96\u0026thinsp;\u0026plusmn;\u0026thinsp;0.12, Urban High: 1.01\u0026thinsp;\u0026plusmn;\u0026thinsp;0.12), and highest in the suburban medium and high-income neighborhoods (Suburban Medium: 1.81\u0026thinsp;\u0026plusmn;\u0026thinsp;0.12, Suburban High: 2.24\u0026thinsp;\u0026plusmn;\u0026thinsp;0.12). Predator abundances were lowest in the urban low-income neighborhood (Urban Low: 0.00\u0026thinsp;\u0026plusmn;\u0026thinsp;0.16), intermediate in the urban medium and high and suburban low and medium-income neighborhoods (Urban Medium: 0.54\u0026thinsp;\u0026plusmn;\u0026thinsp;0.26, Urban High: 0.78\u0026thinsp;\u0026plusmn;\u0026thinsp;0.15, Suburban Low: 1.12\u0026thinsp;\u0026plusmn;\u0026thinsp;0.14, Suburban Medium: 0.68\u0026thinsp;\u0026plusmn;\u0026thinsp;0.15), and highest in the suburban high-income neighborhood (Suburban High: 1.94\u0026thinsp;\u0026plusmn;\u0026thinsp;0.14).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"4. Discussion","content":"\u003cp\u003eWe observed significant differences in arthropod abundances across urban and suburban areas, with greater abundances of both herbivores and predators in high and medium-income suburban areas. Specifically, we found fewer herbivores in low-income areas (urban and suburban), followed by urban medium- and high-income areas, and finally suburban medium- and high-income areas had the highest herbivore abundances. Similarly, the fewest predators were found in urban low-income areas and the most in suburban high-income areas. Altogether, we found that arthropods have higher abundances in suburban locations than in urban ones, indicating that urbanization might decrease arthropod abundance. One might say there are more bugs in the burbs.\u003c/p\u003e \u003cp\u003eOur findings indicate that natural forested areas experience significantly greater average herbivorous insect damage than suburban and urban locations, with more zero-damage leaves in urban\u0026thinsp;\u0026gt;\u0026thinsp;suburban\u0026thinsp;\u0026gt;\u0026thinsp;forest. This is consistent with recent research (Bode \u0026amp; Gilbert, \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Herrmann et al., \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Kozlov et al., \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Moreira et al., \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Schueller et al., \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), which has found decreased insect herbivory with increasing urbanization, thus contributing to a growing body of literature that contradicts past findings that herbivory increases with urbanization (Cuevas-Reyes et al., \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Dreistadt et al., \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e1990\u003c/span\u003e; Raupp et al., \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). Additionally, our study adds a layer of complexity by investigating the impacts of average neighborhood income on leaf damage and arthropod abundances, complicating the urbanization gradient. While we found more zero-damage leaves in medium and high-income urban areas, when excluding zero-damage leaves, we surprisingly found higher average damage on different ends of the income spectrum: suburban high-income (Travilah) and urban low-income areas (Anacostia) had leaves with the greatest herbivore damage.\u003c/p\u003e \u003cp\u003eOur arthropod abundance findings contradict the literature, which cites herbivore abundance increasing as urbanization increases, typically attributed to human-caused characteristics of urbanized areas, such as higher temperatures (Just et al., \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Raupp et al., \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Youngsteadt et al., \u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). However, this is not the case in our study, as we found lower levels of herbivores in urban areas. This disparity may partly be explained by differences across income levels in our study. We found that low-income areas (Anacostia and White Oak) had the lowest herbivore abundances, followed by middle and high-income sites in Washington DC and middle and high-income suburban sites within Montgomery County, Maryland. Predator abundances showed a relatively similar trend to herbivores, with high-income suburban areas having the highest abundance, while the low-income urban area, Anacostia, had significantly lower predator abundance.\u003c/p\u003e \u003cp\u003eA factor that could impact herbivore abundance is the difference in habitat availability between urban and suburban locations. On average, urban areas in the DC metropolitan area have less tree coverage and green space than suburban areas, with the suburbs having almost two times the tree coverage compared to the urban areas (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Decreased habitat availability can lead to overcrowding of arthropods on individual trees. Similarly, habitat fragmentation and physical barriers (buildings) may make it difficult for many arthropod species to migrate among trees (Fenoglio et al., \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). This can result in increased competition between urban-dwelling arthropods as fewer habitats are present and accessible. In contrast, a higher number and density of trees in the suburbs could increase arthropod survival and abundance.\u003c/p\u003e \u003cp\u003eAdditionally, streets and sidewalks confine urban street trees into small regulated grids of soil that reduce nutrient and water uptake by limiting space and increasing soil compaction (Dale \u0026amp; Frank, \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2014b\u003c/span\u003e). This nutrient and water stress impacts street trees (Berrang et al., \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e1985\u003c/span\u003e) and in turn may impact the herbivorous insects feeding on them. For example, armored-scale insect survival and abundance declines with increasing water stress on street trees (Cockfield \u0026amp; Potter, \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e1986\u003c/span\u003e; Hanks \u0026amp; Denno, \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e1993\u003c/span\u003e). In addition, impervious surface cover can impact arthropod abundance, with differential impacts based on guild. Penone et al. (\u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2013\u003c/span\u003e) found that mobile Orthopterans were more sensitive to increased impervious surface cover compared to sedentary species. The difference in herbivore abundance in our study compared to the previous literature might be due to these characteristics (ISC and tree cover), as suburban environments tend to be more similar to natural areas and thus may lend themselves to higher arthropod abundance than urban areas.\u003c/p\u003e \u003cp\u003eOur results showed that herbivory levels decreased as urbanization increased, which is contradictory to past consensus (Cuevas-Reyes et al., \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Dreistadt et al., \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e1990\u003c/span\u003e; Raupp et al., \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2010\u003c/span\u003e), but is in line with a growing body of recent research finding herbivory to decrease with urbanization (Bode \u0026amp; Gilbert, \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Herrmann et al., \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Kozlov et al., \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Moreira et al., \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Schueller et al., \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Because we found similar patterns of herbivore and predator abundances within urban and suburban area types, there is a low likelihood that the level of damage can be attributed to top-down controls (\u003cem\u003ei.e.\u003c/em\u003e, predator abundance controlling herbivore abundance). Instead, the low levels of herbivory in urban areas in our study might be attributed to bottom-up controlling factors common to urban environments. Irrigation and pruning result in foliage with increased nitrogen and decreased secondary defense compounds (Raupp et al., \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2010\u003c/span\u003e), while increased carbon dioxide and nitrogen levels are associated with lower defense levels (Moreira et al., \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Fossil fuel pollution from transportation, runoff due to high impervious surface coverage (\u003cem\u003ee.g.\u003c/em\u003e, Brightwood and Georgetown with around 60% impervious surface cover) or direct fertilizer application all lead to increased nitrogen content of plants, increasing leaf nutrient quality. Counterintuitively, this increased leaf quality in urban areas may lead to lower levels of herbivory, as herbivores can each consume less per capita and still fulfill their nutritional needs (Kozlov et al., \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; La Pierre \u0026amp; Smith, \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2016\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eWhile the low-income urban area of Anacostia did not follow the same pattern as the other urban sites (decreased herbivory in urban areas), our results do support our prediction that low-income areas would experience higher levels of herbivory. Interestingly, we found the same level of herbivory in low-income Anacostia as in Travilah, the suburban neighborhood with the highest average median household income in our study. This interesting pattern of highest herbivory in the high-income suburbs (Travilah) and low-income urban area (Anacostia) may be related to variations in tree coverage and the uniqueness of DC as an urban city. With the highest tree coverage (63%) and lowest impervious surface coverage (7%; Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e), Travilah has environmental conditions that are more similar to natural forested trees, especially considering that wooded areas surround the neighborhood. High herbivore rates may stem from a \u0026ldquo;spillover effect\u0026rdquo; of herbivorous insects from nearby natural forested areas. With growing habitat fragmentation and increased agricultural land use, many studies are investigating the impacts of spillover from natural to managed and managed to natural ecosystems related to herbivores and pests (Blitzer et al., \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2012\u003c/span\u003e) or pathogens such as Ebola and the coronavirus (Alexander et al., \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). To this point, Georgetown, which has considerably lower tree coverage and higher impervious surface coverage than Travilah (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e), looks and feels like a typical cityscape, with the neighborhood featuring a variety of high-end stores and restaurants. As such, for Georgetown higher income does not equate to more tree coverage. In contrast, while Anacostia residents have the lowest average median household income, they live with higher tree coverage and less impervious surface coverage than Georgetown (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Additionally, Anacostia, similarly to Travilah, has multiple parks within and adjacent to the neighborhood. This green space could explain the similarity between rates of herbivory in Anacostia and Travilah, as the same mechanisms of similarity to forested areas and spillover could be responsible.\u003c/p\u003e \u003cp\u003eThe health of urban street trees is significant in the context of urban warming, increased pollution, and decreased rainfall, all of which couple with variations in herbivory to impact the ecosystem services street trees provide humans. Street trees play important roles in urban and suburban areas. Urbanization results in more buildings and paved roads, contributing to the urban island heat effect (Arnfield, \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Freedman, \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e1995\u003c/span\u003e; Oke \u0026amp; Maxwell, \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e1975\u003c/span\u003e; Price, \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e1979\u003c/span\u003e) and increased runoff of pollutants (Haughton \u0026amp; Hunter, \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2004\u003c/span\u003e). Vegetated areas with plants and street trees help lower temperatures (Armson et al., \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2012\u003c/span\u003e), absorb runoff (Bolund \u0026amp; Hunhammar, \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e1999\u003c/span\u003e), and reduce the energy usage of surrounding houses and neighborhoods (Huang et al., \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). Considering all the benefits urban street trees provide residents, especially those in low-income neighborhoods, it is important to understand the ecology of street trees in suburban and urban ecosystems. Our results demonstrate the important role of urbanization, income level, and factors such as impervious surface and tree canopy coverage in structuring plant-herbivorous insect interactions, which can help inform street tree management in the future (Dale \u0026amp; Frank, \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2017\u003c/span\u003e).\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAcknowledgements\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eFunding was provided by the National Science Foundation Grant #NSF DBI 1950656\u003c/p\u003e\n\u003cp\u003eto A. Cawood and J. Parker for SERC\u0026apos;s Research Experience for Undergraduates program for E. Blake\u0026rsquo;s REU experience to conduct this research.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003e\u003cstrong\u003eAuthor Contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll authors contributed to the study conception and design. EB, SB, and AH conducted the field research. EB, AH, and KK conducted the statistical analyses. EB wrote the first manuscript draft, with revisions from all authors. All authors have read and approved the final manuscript.\u003c/p\u003e\n\u003cp\u003e\u0026nbsp;\u003cstrong\u003eCompeting Interests Statement:\u003c/strong\u003e The authors have no relevant financial or non-financial interests to disclose.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAlexander, K. A., Carlson, C. J., Lewis, B. L., Getz, W. M., Marathe, M. V., Eubank, S. G., Sanderson, C. E., \u0026amp; Blackburn, J. K. (2018). The Ecology of Pathogen Spillover and Disease Emergence at the Human-Wildlife-Environment Interface. In C. J. Hurst (Ed.), \u003cem\u003eThe Connections Between Ecology and Infectious Disease\u003c/em\u003e (pp. 267-298). Springer International Publishing. https://doi.org/10.1007/978-3-319-92373-4_8 \u003c/li\u003e\n\u003cli\u003eAlvey, A. A. (2006). Promoting and preserving biodiversity in the urban forest. \u003cem\u003eUrban Forestry \u0026amp;amp; Urban Greening\u003c/em\u003e,\u003cem\u003e 5\u003c/em\u003e(4), 195-201. https://doi.org/10.1016/j.ufug.2006.09.003 \u003c/li\u003e\n\u003cli\u003eArmson, D., Stringer, P., \u0026amp; Ennos, A. R. (2012). The effect of tree shade and grass on surface and globe temperatures in an urban area. \u003cem\u003eUrban Forestry \u0026amp; Urban Greening\u003c/em\u003e,\u003cem\u003e 11\u003c/em\u003e(3), 245-255. https://doi.org/https://doi.org/10.1016/j.ufug.2012.05.002 \u003c/li\u003e\n\u003cli\u003eArnfield, A. J. (2003). Two decades of urban climate research: a review of turbulence, exchanges of energy and water, and the urban heat island. \u003cem\u003eInternational Journal of Climatology\u003c/em\u003e,\u003cem\u003e 23\u003c/em\u003e(1), 1-26. https://doi.org/https://doi.org/10.1002/joc.859 \u003c/li\u003e\n\u003cli\u003eBagchi, R., Gallery, R. E., Gripenberg, S., Gurr, S. J., Narayan, L., Addis, C. E., Freckleton, R. P., \u0026amp; Lewis, O. T. (2014). Pathogens and insect herbivores drive rainforest plant diversity and composition. \u003cem\u003eNature\u003c/em\u003e,\u003cem\u003e 506\u003c/em\u003e(7486), 85-88. https://doi.org/10.1038/nature12911 \u003c/li\u003e\n\u003cli\u003eBates, D., M\u0026auml;chler, M., Bolker, B., \u0026amp; Walker, S. (2015). Fitting Linear Mixed-Effects Models Using lme4. \u003cem\u003eJournal of Statistical Software\u003c/em\u003e,\u003cem\u003e 67\u003c/em\u003e(1), 1 - 48. https://doi.org/10.18637/jss.v067.i01 \u003c/li\u003e\n\u003cli\u003eBeecham, S., \u0026amp; Lucke, T. (2015). Street Trees in Paved Urban Environments: The Benefits and Challenges. Proceeding of the 16th National Street Tree Symposium, \u003c/li\u003e\n\u003cli\u003eBerrang, P., Karnosky, D. F., \u0026amp; Stanton, B. J. (1985). Environmental Factors Affecting Tree Health in New York City. \u003cem\u003eArboriculture \u0026amp;amp; Urban Forestry (AUF)\u003c/em\u003e,\u003cem\u003e 11\u003c/em\u003e(6), 185-189. https://doi.org/10.48044/jauf.1985.042 \u003c/li\u003e\n\u003cli\u003eBigger, D. S., \u0026amp; Marvier, M. A. (1998). How different would a world without herbivory be?: A search for generality in ecology. \u003cem\u003eIntegrative Biology: Issues, News, and Reviews\u003c/em\u003e,\u003cem\u003e 1\u003c/em\u003e(2), 60-67. https://doi.org/10.1002/(sici)1520-6602(1998)1:2\u0026lt;60::aid-inbi4\u0026gt;3.0.co;2-z \u003c/li\u003e\n\u003cli\u003eBj\u0026ouml;rkman, C., Dalin, P., \u0026amp; Ahrn\u0026eacute;, K. (2008). Leaf trichome responses to herbivory in willows: induction, relaxation and costs. \u003cem\u003eNew Phytologist\u003c/em\u003e,\u003cem\u003e 179\u003c/em\u003e(1), 176-184. https://doi.org/10.1111/j.1469-8137.2008.02442.x \u003c/li\u003e\n\u003cli\u003eBlitzer, E. J., Dormann, C. F., Holzschuh, A., Klein, A.-M., Rand, T. A., \u0026amp; Tscharntke, T. (2012). Spillover of functionally important organisms between managed and natural habitats. \u003cem\u003eAgriculture, Ecosystems \u0026amp; Environment\u003c/em\u003e,\u003cem\u003e 146\u003c/em\u003e(1), 34-43. https://doi.org/https://doi.org/10.1016/j.agee.2011.09.005 \u003c/li\u003e\n\u003cli\u003eBode, R. F., \u0026amp; Gilbert, A. B. (2015). Seed Predators, not Herbivores, Exert Natural Selection on Solidago spp . in an Urban Archipelago. \u003cem\u003eEnvironmental Entomology\u003c/em\u003e,\u003cem\u003e 45\u003c/em\u003e(1), 150-154. https://doi.org/10.1093/ee/nvv158 \u003c/li\u003e\n\u003cli\u003eBolund, P., \u0026amp; Hunhammar, S. (1999). Ecosystem services in urban areas. \u003cem\u003eEcological Economics\u003c/em\u003e,\u003cem\u003e 29\u003c/em\u003e(2), 293-301. https://doi.org/https://doi.org/10.1016/S0921-8009(99)00013-0 \u003c/li\u003e\n\u003cli\u003eBrooks, M. E., Kristensen, K., Van Benthem, K. J., Magnusson, A., Berg, C. W., Nielsen, A., Skaug, H. J., Machler, M., \u0026amp; Bolker, B. M. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. \u003cem\u003eThe R journal\u003c/em\u003e,\u003cem\u003e 9\u003c/em\u003e(2), 378-400. \u003c/li\u003e\n\u003cli\u003eCabrera, H. M., Argando\u0026ntilde;a, V. H., \u0026amp; Corcuera, L. J. (1994). Metabolic changes in barley seedlings at different aphid infestation levels. \u003cem\u003ePhytochemistry\u003c/em\u003e,\u003cem\u003e 35\u003c/em\u003e(2), 317-319. https://doi.org/10.1016/s0031-9422(00)94755-1 \u003c/li\u003e\n\u003cli\u003eChakraborty, T., Hsu, A., Manya, D., \u0026amp; Sheriff, G. (2019). Disproportionately higher exposure to urban heat in lower-income neighborhoods: a multi-city perspective. \u003cem\u003eEnvironmental Research Letters\u003c/em\u003e,\u003cem\u003e 14\u003c/em\u003e(10), 105003. https://doi.org/10.1088/1748-9326/ab3b99 \u003c/li\u003e\n\u003cli\u003eChaves, M. M., Flexas, J., \u0026amp; Pinheiro, C. (2009). Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. \u003cem\u003eAnnals of Botany\u003c/em\u003e,\u003cem\u003e 103\u003c/em\u003e(4), 551-560. https://doi.org/10.1093/aob/mcn125 \u003c/li\u003e\n\u003cli\u003eCockfield, S. D., \u0026amp; Potter, D. A. (1986). Interaction of Euonymus scale (Homoptera: Diaspididae) feeding damage and severe water stress on leaf abscission and growth of Euonymus fortunei. \u003cem\u003eOecologia\u003c/em\u003e,\u003cem\u003e 71\u003c/em\u003e(1), 41-46. https://doi.org/10.1007/BF00377318 \u003c/li\u003e\n\u003cli\u003eCrawley, M. J. (1989). Insect Herbivores and Plant Population Dynamics. \u003cem\u003eAnnual Review of Entomology\u003c/em\u003e,\u003cem\u003e 34\u003c/em\u003e(1), 531-562. https://doi.org/10.1146/annurev.en.34.010189.002531 \u003c/li\u003e\n\u003cli\u003eCuevas-Reyes, P., Gilberti, L., Gonz\u0026aacute;lez-Rodr\u0026iacute;guez, A., \u0026amp; Fernandes, G. W. (2013). Patterns of herbivory and fluctuating asymmetry in Solanum lycocarpum St. Hill (Solanaceae) along an urban gradient in Brazil. \u003cem\u003eEcological Indicators\u003c/em\u003e,\u003cem\u003e 24\u003c/em\u003e, 557-561. https://doi.org/https://doi.org/10.1016/j.ecolind.2012.08.011 \u003c/li\u003e\n\u003cli\u003eDale, A. G., \u0026amp; Frank, S. D. (2014a). Urban warming trumps natural enemy regulation of herbivorous pests. \u003cem\u003eEcological Applications\u003c/em\u003e,\u003cem\u003e 24\u003c/em\u003e(7), 1596-1607. https://doi.org/https://doi.org/10.1890/13-1961.1 \u003c/li\u003e\n\u003cli\u003eDale, A. G., \u0026amp; Frank, S. D. (2014b). The Effects of Urban Warming on Herbivore Abundance and Street Tree Condition. \u003cem\u003ePLOS ONE\u003c/em\u003e,\u003cem\u003e 9\u003c/em\u003e(7), e102996. https://doi.org/10.1371/journal.pone.0102996 \u003c/li\u003e\n\u003cli\u003eDale, A. G., \u0026amp; Frank, S. D. (2017). Warming and drought combine to increase pest insect fitness on urban trees. \u003cem\u003ePLOS ONE\u003c/em\u003e,\u003cem\u003e 12\u003c/em\u003e(3), e0173844. https://doi.org/10.1371/journal.pone.0173844 \u003c/li\u003e\n\u003cli\u003eDonovan, G. H., \u0026amp; Butry, D. T. (2010). Trees in the city: Valuing street trees in Portland, Oregon. \u003cem\u003eLandscape and Urban Planning\u003c/em\u003e,\u003cem\u003e 94\u003c/em\u003e(2), 77-83. https://doi.org/10.1016/j.landurbplan.2009.07.019 \u003c/li\u003e\n\u003cli\u003eDreistadt, S. H., Dahlsten, D. L., \u0026amp; Frankie, G. W. (1990). Urban Forests and Insect Ecology. \u003cem\u003eBioScience\u003c/em\u003e,\u003cem\u003e 40\u003c/em\u003e(3), 192-198. https://doi.org/10.2307/1311364 \u003c/li\u003e\n\u003cli\u003eFelson, A. J., Bradford, M. A., \u0026amp; Terway, T. M. (2013). Promoting Earth Stewardship through urban design experiments. \u003cem\u003eFrontiers in Ecology and the Environment\u003c/em\u003e,\u003cem\u003e 11\u003c/em\u003e(7), 362-367. https://doi.org/10.1890/130061 \u003c/li\u003e\n\u003cli\u003eFenoglio, M. S., Calvi\u0026ntilde;o, A., Gonz\u0026aacute;lez, E., Salvo, A., \u0026amp; Videla, M. (2021). Urbanisation drivers and underlying mechanisms of terrestrial insect diversity loss in cities. \u003cem\u003eEcological Entomology\u003c/em\u003e,\u003cem\u003e 46\u003c/em\u003e(4), 757-771. https://doi.org/https://doi.org/10.1111/een.13041 \u003c/li\u003e\n\u003cli\u003eFreedman, B. (1995). 1 - THE ECOLOGICAL EFFECTS OF POLLUTION, DISTURBANCE, AND OTHER STRESSES. In B. Freedman (Ed.), \u003cem\u003eEnvironmental Ecology (Second Edition)\u003c/em\u003e (pp. 1-10). Academic Press. https://doi.org/https://doi.org/10.1016/B978-0-08-050577-0.50006-6 \u003c/li\u003e\n\u003cli\u003eGetman-Pickering, Z. L., Campbell, A., Aflitto, N., Grele, A., Davis, J. K., \u0026amp; Ugine, T. A. (2020). LeafByte: A mobile application that measures leaf area and herbivory quickly and accurately. \u003cem\u003eMethods in Ecology and Evolution\u003c/em\u003e,\u003cem\u003e 11\u003c/em\u003e(2), 215-221. https://doi.org/https://doi.org/10.1111/2041-210X.13340 \u003c/li\u003e\n\u003cli\u003eHanks, L. M., \u0026amp; Denno, R. F. (1993). Natural Enemies and Plant Water Relations Influence the Distribution of an Armored Scale Insect. \u003cem\u003eEcology\u003c/em\u003e,\u003cem\u003e 74\u003c/em\u003e(4), 1081-1091. https://doi.org/https://doi.org/10.2307/1940478 \u003c/li\u003e\n\u003cli\u003eHaughton, G., \u0026amp; Hunter, C. (2004). \u003cem\u003eSustainable cities\u003c/em\u003e. Routledge. \u003c/li\u003e\n\u003cli\u003eHerrmann, D. L., Pearse, I. S., \u0026amp; Baty, J. H. (2012). Drivers of specialist herbivore diversity across 10 cities. \u003cem\u003eLandscape and Urban Planning\u003c/em\u003e,\u003cem\u003e 108\u003c/em\u003e(2), 123-130. https://doi.org/https://doi.org/10.1016/j.landurbplan.2012.08.007 \u003c/li\u003e\n\u003cli\u003eHilbert, D., Roman, L., Koeser, A., Vogt, J., \u0026amp; Van Doorn, N. (2018). \u003cem\u003eUrban Tree Mortality: A Literature Review\u003c/em\u003e. https://doi.org/10.13140/RG.2.2.25953.15204 \u003c/li\u003e\n\u003cli\u003eHoffman, J. S., Shandas, V., \u0026amp; Pendleton, N. (2020). The effects of historical housing policies on resident exposure to intra-urban heat: a study of 108 US urban areas. \u003cem\u003eClimate\u003c/em\u003e,\u003cem\u003e 8\u003c/em\u003e(1), 12. \u003c/li\u003e\n\u003cli\u003eHsu, A., Sheriff, G., Chakraborty, T., \u0026amp; Manya, D. (2021). Disproportionate exposure to urban heat island intensity across major US cities. \u003cem\u003eNature Communications\u003c/em\u003e,\u003cem\u003e 12\u003c/em\u003e(1), 2721. https://doi.org/10.1038/s41467-021-22799-5 \u003c/li\u003e\n\u003cli\u003eHuang, G., Zhou, W., \u0026amp; Cadenasso, M. L. (2011). Is everyone hot in the city? Spatial pattern of land surface temperatures, land cover and neighborhood socioeconomic characteristics in Baltimore, MD. \u003cem\u003eJournal of Environmental Management\u003c/em\u003e,\u003cem\u003e 92\u003c/em\u003e(7), 1753-1759. https://doi.org/https://doi.org/10.1016/j.jenvman.2011.02.006 \u003c/li\u003e\n\u003cli\u003eJohnson, S. N., Erb, M., \u0026amp; Hartley, S. E. (2016). Roots under attack: contrasting plant responses to below‐ and aboveground insect herbivory. \u003cem\u003eNew Phytologist\u003c/em\u003e,\u003cem\u003e 210\u003c/em\u003e(2), 413-418. https://doi.org/10.1111/nph.13807 \u003c/li\u003e\n\u003cli\u003eJust, M. G., Dale, A. G., Long, L. C., \u0026amp; Frank, S. D. (2019). Urbanization drives unique latitudinal patterns of insect herbivory and tree condition. \u003cem\u003eOikos\u003c/em\u003e,\u003cem\u003e 128\u003c/em\u003e(7), 984-993. https://doi.org/https://doi.org/10.1111/oik.05874 \u003c/li\u003e\n\u003cli\u003eKaakeh, W., Pfeiffer, D. G., \u0026amp; Marini, R. P. (1992). Combined Effects of Spirea Aphid (Homoptera: Aphididae) and Nitrogen Fertilization on Net Photosynthesis, Total Chlorophyll Content, and Greenness of Apple Leaves. \u003cem\u003eJournal of Economic Entomology\u003c/em\u003e,\u003cem\u003e 85\u003c/em\u003e(3), 939-946. https://doi.org/10.1093/jee/85.3.939 \u003c/li\u003e\n\u003cli\u003eKozlov, M. V., Lanta, V., x11b, ch, Zverev, V. E., \u0026amp; Zvereva, E. L. (2012). Delayed local responses of downy birch to damage by leafminers and leafrollers. \u003cem\u003eOikos\u003c/em\u003e,\u003cem\u003e 121\u003c/em\u003e(3), 428-434. http://www.jstor.org/stable/41428987 \u003c/li\u003e\n\u003cli\u003eKozlov, M. V., Lanta, V., Zverev, V., Rainio, K., Kunavin, M. A., \u0026amp; Zvereva, E. L. (2017). Decreased losses of woody plant foliage to insects in large urban areas are explained by bird predation. \u003cem\u003eGlobal Change Biology\u003c/em\u003e,\u003cem\u003e 23\u003c/em\u003e(10), 4354-4364. https://doi.org/https://doi.org/10.1111/gcb.13692 \u003c/li\u003e\n\u003cli\u003eKozlov, M. V., Lanta, V., Zverev, V., \u0026amp; Zvereva, E. L. (2015). Global patterns in background losses of woody plant foliage to insects. \u003cem\u003eGlobal Ecology and Biogeography\u003c/em\u003e,\u003cem\u003e 24\u003c/em\u003e(10), 1126-1135. https://doi.org/10.1111/geb.12347 \u003c/li\u003e\n\u003cli\u003eKozlov, M. V., Zverev, V., \u0026amp; Zvereva, E. L. (2014). Confirmation bias leads to overestimation of losses of woody plant foliage to insect herbivores in tropical regions. \u003cem\u003ePeerJ\u003c/em\u003e,\u003cem\u003e 2\u003c/em\u003e, e709. https://doi.org/10.7717/peerj.709 \u003c/li\u003e\n\u003cli\u003eKozlov, M. V., \u0026amp; Zvereva, E. L. (2018). Background Insect Herbivory: Impacts, Patterns and Methodology. In F. M. C\u0026aacute;novas, U. L\u0026uuml;ttge, \u0026amp; R. Matyssek (Eds.), \u003cem\u003eProgress in Botany Vol. 79\u003c/em\u003e (pp. 313-355). Springer International Publishing. https://doi.org/10.1007/124_2017_4 \u003c/li\u003e\n\u003cli\u003eLa Pierre, K. J., \u0026amp; Smith, M. D. (2016). Soil nutrient additions increase invertebrate herbivore abundances, but not herbivory, across three grassland systems. \u003cem\u003eOecologia\u003c/em\u003e,\u003cem\u003e 180\u003c/em\u003e(2), 485-497. https://doi.org/10.1007/s00442-015-3471-7 \u003c/li\u003e\n\u003cli\u003eLahr, E. C., Dunn, R. R., \u0026amp; Frank, S. D. (2018). Variation in photosynthesis and stomatal conductance among red maple (Acer rubrum) urban planted cultivars and wildtype trees in the southeastern United States. \u003cem\u003ePLOS ONE\u003c/em\u003e,\u003cem\u003e 13\u003c/em\u003e(5), e0197866. https://doi.org/10.1371/journal.pone.0197866 \u003c/li\u003e\n\u003cli\u003eLamarre, G. P. A., Baraloto, C., Fortunel, C., D\u0026aacute;vila, N., Mesones, I., Rios, J. G., R\u0026iacute;os, M., Valderrama, E., Pilco, M. V., \u0026amp; Fine, P. V. A. (2012). Herbivory, growth rates, and habitat specialization in tropical tree lineages: implications for Amazonian beta-diversity. \u003cem\u003eEcology\u003c/em\u003e,\u003cem\u003e 93\u003c/em\u003e(8), S195-S210. http://www.jstor.org/stable/23229916 \u003c/li\u003e\n\u003cli\u003eLandry, S. M., \u0026amp; Chakraborty, J. (2009). Street Trees and Equity: Evaluating the Spatial Distribution of an Urban Amenity. \u003cem\u003eEnvironment and Planning A: Economy and Space\u003c/em\u003e,\u003cem\u003e 41\u003c/em\u003e(11), 2651-2670. https://doi.org/10.1068/a41236 \u003c/li\u003e\n\u003cli\u003eMarquis, R. J., \u0026amp; Whelan, C. J. (1994). Insectivorous Birds Increase Growth of White Oak through Consumption of Leaf-Chewing Insects. \u003cem\u003eEcology\u003c/em\u003e,\u003cem\u003e 75\u003c/em\u003e(7), 2007-2014. https://doi.org/10.2307/1941605 \u003c/li\u003e\n\u003cli\u003eMetcalfe, D. B., Asner, G. P., Martin, R. E., Silva Espejo, J. E., Huasco, W. H., Farf\u0026aacute;n Am\u0026eacute;zquita, F. F., Carranza‐Jimenez, L., Galiano Cabrera, D. F., Baca, L. D., Sinca, F., Huaraca Quispe, L. P., Taype, I. A., Mora, L. E., D\u0026aacute;vila, A. R., Sol\u0026oacute;rzano, M. M., Puma Vilca, B. L., Laupa Rom\u0026aacute;n, J. M., Guerra Bustios, P. C., Revilla, N. S., . . . Malhi, Y. (2014). Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. \u003cem\u003eEcology Letters\u003c/em\u003e,\u003cem\u003e 17\u003c/em\u003e(3), 324-332. https://doi.org/10.1111/ele.12233 \u003c/li\u003e\n\u003cli\u003eMoreira, X., Abdala-Roberts, L., Berny Mier y Teran, J. C., Covelo, F., de la Mata, R., Francisco, M., Hardwick, B., Pires, R. M., Roslin, T., Schigel, D. S., ten Hoopen, J. P. J. G., Timmermans, B. G. H., van Dijk, L. J. A., Castagneyrol, B., \u0026amp; Tack, A. J. M. (2019). Impacts of urbanization on insect herbivory and plant defences in oak trees. \u003cem\u003eOikos\u003c/em\u003e,\u003cem\u003e 128\u003c/em\u003e(1), 113-123. https://doi.org/https://doi.org/10.1111/oik.05497 \u003c/li\u003e\n\u003cli\u003eMullaney, J., Lucke, T., \u0026amp; Trueman, S. J. (2015). A review of benefits and challenges in growing street trees in paved urban environments. \u003cem\u003eLandscape and Urban Planning\u003c/em\u003e,\u003cem\u003e 134\u003c/em\u003e, 157-166. https://doi.org/10.1016/j.landurbplan.2014.10.013 \u003c/li\u003e\n\u003cli\u003eNabity, P. D., Zavala, J. A., \u0026amp; Delucia, E. H. (2009). Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. \u003cem\u003eAnnals of Botany\u003c/em\u003e,\u003cem\u003e 103\u003c/em\u003e(4), 655-663. https://doi.org/10.1093/aob/mcn127 \u003c/li\u003e\n\u003cli\u003eNational Wildlife Federation. \u003cem\u003eRed Maple\u003c/em\u003e. https://www.nwf.org/Home/Educational-Resources/Wildlife-Guide/Plants-and-Fungi/Red-Maple\u003c/li\u003e\n\u003cli\u003eOke, T. R., \u0026amp; Maxwell, G. B. (1975). Urban heat island dynamics in Montreal and Vancouver. \u003cem\u003eAtmospheric Environment (1967)\u003c/em\u003e,\u003cem\u003e 9\u003c/em\u003e(2), 191-200. https://doi.org/https://doi.org/10.1016/0004-6981(75)90067-0 \u003c/li\u003e\n\u003cli\u003ePataki, D. E., Alberti, M., Cadenasso, M. L., Felson, A. J., McDonnell, M. J., Pincetl, S., Pouyat, R. V., Set\u0026auml;l\u0026auml;, H., \u0026amp; Whitlow, T. H. (2021). The Benefits and Limits of Urban Tree Planting for Environmental and Human Health. \u003cem\u003eFrontiers in Ecology and Evolution\u003c/em\u003e,\u003cem\u003e 9\u003c/em\u003e. https://doi.org/10.3389/fevo.2021.603757 \u003c/li\u003e\n\u003cli\u003ePenone, C., Kerbiriou, C., Julien, J.-F., Julliard, R., Machon, N., \u0026amp; Le Viol, I. (2013). Urbanisation effect on Orthoptera: which scale matters? \u003cem\u003eInsect Conservation and Diversity\u003c/em\u003e,\u003cem\u003e 6\u003c/em\u003e(3), 319-327. https://doi.org/https://doi.org/10.1111/j.1752-4598.2012.00217.x \u003c/li\u003e\n\u003cli\u003ePrice, J. C. (1979). Assessment of the Urban Heat Island Effect Through the Use of Satellite Data. \u003cem\u003eMonthly Weather Review\u003c/em\u003e,\u003cem\u003e 107\u003c/em\u003e(11), 1554-1557. https://doi.org/https://doi.org/10.1175/1520-0493(1979)107\u0026lt;1554:AOTUHI\u0026gt;2.0.CO;2 \u003c/li\u003e\n\u003cli\u003eRaupp, M. J., Shrewsbury, P. M., \u0026amp; Herms, D. A. (2010). Ecology of Herbivorous Arthropods in Urban Landscapes. \u003cem\u003eAnnual Review of Entomology\u003c/em\u003e,\u003cem\u003e 55\u003c/em\u003e(1), 19-38. https://doi.org/10.1146/annurev-ento-112408-085351 \u003c/li\u003e\n\u003cli\u003eSchaffer, B., \u0026amp; Mason, L. J. (1990). Effects of scale insect herbivory and shading on net gas exchange and growth of a subtropical tree species (Guaiacum sanctum L.). \u003cem\u003eOecologia\u003c/em\u003e,\u003cem\u003e 84\u003c/em\u003e(4), 468-473. https://doi.org/10.1007/BF00328162 \u003c/li\u003e\n\u003cli\u003eSchmitt, L., \u0026amp; Burghardt, K. T. (2021). Urbanization as a disrupter and facilitator of insect herbivore behaviors and life cycles. \u003cem\u003eCurrent Opinion in Insect Science\u003c/em\u003e,\u003cem\u003e 45\u003c/em\u003e, 97-105. https://doi.org/https://doi.org/10.1016/j.cois.2021.02.016 \u003c/li\u003e\n\u003cli\u003eSchueller, S. K., Paul, S., Payer, N., Schultze, R., \u0026amp; Vikas, M. (2019). Urbanization decreases the extent and variety of leaf herbivory for native canopy tree species Quercus rubra, Quercus alba, and Acer saccharum. \u003cem\u003eUrban Ecosystems\u003c/em\u003e,\u003cem\u003e 22\u003c/em\u003e(5), 907-916. https://doi.org/10.1007/s11252-019-00866-6 \u003c/li\u003e\n\u003cli\u003eSoares, A. L., Rego, F. C., McPherson, E. G., Simpson, J. R., Peper, P. J., \u0026amp; Xiao, Q. (2011). Benefits and costs of street trees in Lisbon, Portugal. \u003cem\u003eUrban Forestry \u0026amp;amp; Urban Greening\u003c/em\u003e,\u003cem\u003e 10\u003c/em\u003e(2), 69-78. https://doi.org/10.1016/j.ufug.2010.12.001 \u003c/li\u003e\n\u003cli\u003eThe Herbivory Variability Network, Robinson, M. L., Hahn, P. G., Inouye, B. D., Underwood, N., Whitehead, S. R., Abbott, K. C., Bruna, E. M., Cacho, N. I., Dyer, L. A., Abdala-Roberts, L., Allen, W. J., Andrade, J. F., Angulo, D. F., Anjos, D., Anstett, D. N., Bagchi, R., Bagchi, S., Barbosa, M., . . . Wetzel, W. C. (2023). Plant size, latitude, and phylogeny explain within-population variability in herbivory. \u003cem\u003eScience\u003c/em\u003e,\u003cem\u003e 382\u003c/em\u003e(6671), 679-683. https://doi.org/doi:10.1126/science.adh8830 \u003c/li\u003e\n\u003cli\u003eTurner‐Skoff, J. B., \u0026amp; Cavender, N. (2019). The benefits of trees for livable and sustainable communities. \u003cem\u003ePLANTS, PEOPLE, PLANET\u003c/em\u003e,\u003cem\u003e 1\u003c/em\u003e(4), 323-335. https://doi.org/10.1002/ppp3.39 \u003c/li\u003e\n\u003cli\u003eTurrini, T., Sanders, D., \u0026amp; Knop, E. (2016). Effects of urbanization on direct and indirect interactions in a tri‐trophic system. \u003cem\u003eEcological Applications\u003c/em\u003e,\u003cem\u003e 26\u003c/em\u003e(3), 664-675. https://doi.org/10.1890/14-1787 \u003c/li\u003e\n\u003cli\u003eWalters, R. S., \u0026amp; Yawney, H. W. (1990). Acer rubrum L. Red maple. \u003cem\u003eSilvics of North America\u003c/em\u003e,\u003cem\u003e 2\u003c/em\u003e, 60-69. \u003c/li\u003e\n\u003cli\u003eWelter, S. C. (1989). Arthropod Impact on Plant Gas Exchange. In (pp. 135-164). CRC Press. https://doi.org/10.1201/9780429290916-5 \u003c/li\u003e\n\u003cli\u003eWolf, K. L., Lam, S. T., McKeen, J. K., Richardson, G. R. A., van den Bosch, M., \u0026amp; Bardekjian, A. C. (2020). Urban Trees and Human Health: A Scoping Review. \u003cem\u003eInternational Journal of Environmental Research and Public Health\u003c/em\u003e,\u003cem\u003e 17\u003c/em\u003e(12), 4371. https://www.mdpi.com/1660-4601/17/12/4371 \u003c/li\u003e\n\u003cli\u003eYoung, R. F. (2010). Managing municipal green space for ecosystem services. \u003cem\u003eUrban Forestry \u0026amp; Urban Greening\u003c/em\u003e,\u003cem\u003e 9\u003c/em\u003e(4), 313-321. https://doi.org/https://doi.org/10.1016/j.ufug.2010.06.007 \u003c/li\u003e\n\u003cli\u003eYoungsteadt, E., Dale, A. G., Terando, A. J., Dunn, R. R., \u0026amp; Frank, S. D. (2015). Do cities simulate climate change? A comparison of herbivore response to urban and global warming. \u003cem\u003eGlobal Change Biology\u003c/em\u003e,\u003cem\u003e 21\u003c/em\u003e(1), 97-105. https://doi.org/https://doi.org/10.1111/gcb.12692 \u003c/li\u003e\n\u003cli\u003eZangerl, A. R., Hamilton, J. G., Miller, T. J., Crofts, A. R., Oxborough, K., Berenbaum, M. R., \u0026amp; De Lucia, E. H. (2002). Impact of folivory on photosynthesis is greater than the sum of its holes. \u003cem\u003eProceedings of the National Academy of Sciences\u003c/em\u003e,\u003cem\u003e 99\u003c/em\u003e(2), 1088-1091. https://doi.org/10.1073/pnas.022647099 \u003c/li\u003e\n\u003cli\u003eZvereva, E. L., Zverev, V., \u0026amp; Kozlov, M. V. (2012). Little strokes fell great oaks: minor but chronic herbivory substantially reduces birch growth. \u003cem\u003eOikos\u003c/em\u003e,\u003cem\u003e 121\u003c/em\u003e(12), 2036-2043. http://www.jstor.org/stable/41686695 \u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"urban-ecosystems","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"ueco","sideBox":"Learn more about [Urban Ecosystems](https://www.springer.com/journal/11252)","snPcode":"11252","submissionUrl":"https://submission.nature.com/new-submission/11252/3","title":"Urban Ecosystems","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"land use, urban, suburban, forest, leaf damage, red maple, street trees","lastPublishedDoi":"10.21203/rs.3.rs-4219885/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4219885/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eUrbanization has increased wealth disparity within the United States, impacting the urban landscape and species interactions. In particular, the interactions between street trees and the arthropod communities that live among them may be modified by both human population densities across urban to suburban locations, as well as income levels within these areas. We examined the effect of land use type (urban vs suburban) and median household income on variation in leaf damage and arthropod abundance of red maples (\u003cem\u003eAcer rubrum\u003c/em\u003e) in the District of Columbia metropolitan region. We compared these levels of leaf damage to rates observed in a nearby natural forest. We predicted leaf damage would be positively correlated with urbanization (forested\u0026thinsp;\u0026lt;\u0026thinsp;suburban\u0026thinsp;\u0026lt;\u0026thinsp;urban) and a negative relationship between leaf damage and neighborhood income level (low\u0026thinsp;\u0026gt;\u0026thinsp;medium\u0026thinsp;\u0026gt;\u0026thinsp;high). Instead, we observed higher levels of leaf damage on trees in the forest environment compared to the urban and suburban areas. Leaves from urban medium and high-income areas were less likely to exhibit herbivore damage than those from suburban areas. Of the leaves with any damage, those in urban high-income and suburban low-income areas exhibited the most leaf area missing. These trends may be related to specific factors associated with urbanization and income level, such as tree and impervious surface coverage and pesticide use. This study highlights differences in biotic interactions across individual neighborhoods and the importance of including socio-economic variables (e.g., household income) when examining species interactions in developed environments.\u003c/p\u003e","manuscriptTitle":"Insect herbivory on Acer rubrum varies across income and urbanization gradients in the D.C. metropolitan area","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-04-11 18:34:09","doi":"10.21203/rs.3.rs-4219885/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2024-05-08T23:22:09+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2024-05-08T20:50:35+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2024-05-06T21:12:07+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"09742f2b-9a24-4f11-b3a1-d38b70d0e080","date":"2024-04-21T19:17:29+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"00592f4d-e5eb-483b-813a-cb830fe14176","date":"2024-04-21T11:35:25+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"5d1397f9-16cb-44d1-b489-9533fc44afbc","date":"2024-04-15T15:01:48+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"c4a7f896-fdb2-4022-86d0-d6c9a64aaa29","date":"2024-04-13T17:41:59+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2024-04-13T16:48:17+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-04-08T15:16:27+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2024-04-08T12:09:52+00:00","index":"","fulltext":""},{"type":"submitted","content":"Urban Ecosystems","date":"2024-04-04T21:59:06+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"urban-ecosystems","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"ueco","sideBox":"Learn more about [Urban Ecosystems](https://www.springer.com/journal/11252)","snPcode":"11252","submissionUrl":"https://submission.nature.com/new-submission/11252/3","title":"Urban Ecosystems","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"em","reportingPortfolio":"Springer Hybrid","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"02c03b36-61de-4501-974e-3ab0732f1a4b","owner":[],"postedDate":"April 11th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2024-07-27T00:36:44+00:00","versionOfRecord":{"articleIdentity":"rs-4219885","link":"https://doi.org/10.1007/s11252-024-01584-4","journal":{"identity":"urban-ecosystems","isVorOnly":false,"title":"Urban Ecosystems"},"publishedOn":"2024-07-26 00:36:44","publishedOnDateReadable":"July 26th, 2024"},"versionCreatedAt":"2024-04-11 18:34:09","video":"","vorDoi":"10.1007/s11252-024-01584-4","vorDoiUrl":"https://doi.org/10.1007/s11252-024-01584-4","workflowStages":[]},"version":"v1","identity":"rs-4219885","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4219885","identity":"rs-4219885","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}