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Cite as: C. J. Schell et al., Science 10.1126/science.aay4497 (2020).

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Urban ecosystems encompass complex feedbacks between human activity, built and planted infrastructure, and natural landscapes that drive unique biological processes (1–3). Interactions between social and natural systems produce distinctive biogeochemical and biophysical signatures (4, 5) that alter the demography, life histories, diversity, behaviors, and distributions of non-human species (6, 7). Resultant novel environmental conditions (e.g., urban heat island effects, food subsidies, and environmental pollution) can drive phenotypic shifts, emigration, or extinction within and across animal and plant populations (8, 9). Cities have, accordingly, become foci for research addressing biological responses to novel, rapidly changing environments (8–13). Recent urban ecosystems research can inform sustainable so- lutions promoting biodiversity, human well-being, and urban resilience in the face of global environmental change (3, 14– 16). Leveraging urban ecosystems as conduits of sustainabil- ity, conservation, and innovation, however, requires a comprehensive understanding of the underlying component parts, hierarchical structures, and key drivers of urban functions (Fig. 1) (3, 7, 16, 17).

Since its inception, the field of urban ecology has framed cities as quintessential socio-ecological systems (i.e., complex adaptive systems or coupled human and natural systems), where social processes alter ecological properties that reciprocally influence human societies (18–20). These forma- tive urban ecology models placed human decisions and insti- tutions at the core of urban ecosystems, emphasizing the need to quantify spatial and temporal feedbacks within cities (17, 21). For example, urban Long-Term Ecological Research programs in Phoenix, Arizona and Baltimore, Maryland, USA (i.e., the Central-Arizona Phoenix and Balti- more Ecosystem Study, respectively) have established links between social and ecological systems by overlaying habitat patch types with demographic information like neighbor- hood wealth, housing densities, and impervious surface cover (2, 3, 10, 16).

Socioeconomic status has been a standard metric for many socio-ecological studies, combining multiple social fac- tors, including culture, race, occupation, education, and soci- etal power into a complex aggregated measures (22, 23). Many social variables contributing to socioeconomic status

The ecological and evolutionary consequences of systemic racism in urban environments Christopher J. Schell1*, Karen Dyson2,3, Tracy L. Fuentes2, Simone Des Roches2,4, Nyeema C. Harris5, Danica Sterud Miller1, Cleo A. Woelfle-Erskine6, Max R. Lambert7 1School of Interdisciplinary Arts and Sciences, University of Washington, Tacoma, WA 98402, USA. 2College of Built Environments, University of Washington, Seattle, WA 98195, USA. 3Dendrolytics, Seattle, WA 98195, USA. 4School of Aquatic and Fisheries Sciences, University of Washington, Seattle, WA 98195, USA. 5Applied Wildlife Ecology Lab, Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA. 6School of Marine and Environmental Affairs, College of the Environment, University of Washington, Seattle, WA 98195, USA. 7Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA 94720, USA.

*Corresponding author. Email: [email protected]

Urban areas are dynamic ecological systems defined by interdependent biological, physical, and social components. The emergent structure and heterogeneity of the urban landscape drives the biotic outcomes observed, and such spatial patterns are often attributed to the unequal stratification of wealth and power in human societies. Despite these patterns, few studies effectively consider structural inequalities as drivers of ecological and evolutionary outcomes, instead focusing on indicator variables such as neighborhood wealth. We explicitly integrate ecology, evolution, and social processes to emphasize the relationships binding social inequities, specifically racism, and biological change in urbanized landscapes. We draw on existing research to link racist practices – including residential segregation – to the observed heterogeneous patterns of flora and fauna observed by urban ecologists. As a result, urban ecology and evolution researchers must consider how systems of racial oppression affect the environmental factors driving biological change in cities. Conceptual integration of the social and ecological sciences has amassed considerable scholarship in urban ecology over the past few decades, providing a solid foundation for incorporating environmental justice scholarship into urban ecological and evolutionary research. Such an undertaking is necessary to deconstruct urbanization’s biophysical patterns and processes, inform equitable and anti-racist initiatives promoting justice in urban conservation, and strengthen community resilience to global environmental change.

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and related environmental variability are the result of histor- ical government and societal actions (24, 25). Recent studies have begun to address the varied contributions of several so- cial factors (e.g., race, sex, age) to ecological heterogeneity in cities (25–28). However, social inequality remains understud- ied as a key driver of ecological and evolutionary change in cities (Fig. 1) (15, 21, 24). Social inequality is the unequal dis- tribution or allocation of wealth and resources to specific so- cio-cultural groups. Such imbalances contribute to profound injustices (i.e., social inequities; Fig. 1) that privilege certain individuals over others (29–31). Inequality and inequity dis- proportionately affect which individuals own and access land, functionally restricting the people who become the pri- mary drivers of urban ecosystem structure and function (32, 33).

Urban social inequality stems from historical and contem- porary power imbalances, producing deleterious effects that are often intersectional, involving race, economic class, gen- der, language, sexuality, nationality, ability, religion, and age (34). For example, various ecological attributes in cities are principally governed by the spatial and temporal scale of so- cial inequities (23). For instance, the uneven distribution of urban heat islands (35–39), vegetation and tree canopy cover (27, 28, 40, 41), environmental hazards and pollutants (42– 46), access to healthy waterways (47, 48), and the relative pro- portion of native to introduced species (49, 50) are strongly dictated by structural racism and classism (Fig. 1) (21, 31, 32, 51). Concurrently, the environmental justice literature has long articulated the economic, health, and environmental im- plications of structural racism in cities (52–55). Integrating the contributions of social inequities to urban environmental structure is therefore crucial for informing our understand- ing of biological processes in cities (33, 55, 56).

We provide a transdisciplinary synthesis on how social in- equities – and specifically, systemic racism – serve as princi- ple drivers of ecological and evolutionary processes by shaping landscape heterogeneity (Fig. 1). Critically, we draw on the social and political sciences to specifically stress how understanding systemic racism and racial oppression, rooted in settler colonialism and white supremacy, is essential for advancing urban ecology and evolutionary biology research. First, we review the socio-ecological effects of wealth dispar- ities in cities. Second, we describe how systemic racism drive inequitable patterns in wealth, health, and environmental heterogeneity, noting that intersectionality with other identi- ties (e.g., gender, sexual orientation, and Indigeneity) may have additive impacts on urban structure (29, 34, 57). We pro- pose hypotheses linking systemic racism to urban ecological and evolutionary patterns and processes. We close by illus- trating how centering environmental justice and anti-racist activism in biological research is a priority for urban conser- vation (55, 56).

While we predominantly focus on work from North Amer- ica, the global ubiquity of social inequality and systemic rac- ism across cities suggests our synthesis is broadly applicable (58–60). Addressing systemic and structural racism both in cities and in the scientific community is necessary to compre- hensively understand urban ecological and evolutionary dy- namics, conserve biodiversity, improve human health and well-being, and promote justice in nature and society. Socio-ecological effects of wealth Variation in household and neighborhood wealth are cur- rently the most commonly-explored social variables ecol- ogists use to describe within-city biodiversity patterns, especially in residential neighborhoods (26, 61–64). Wealth, specifically median household income, has repeatedly emerged as a significant explanatory variable for predicting urban ecological patterns. One of the most well-known and robust hypotheses linking household income and ecology – the luxury effect – suggests that urban biodiversity, and plant diversity in particular, is positively correlated with neighbor- hood wealth (61, 63).

The wealth-biodiversity covariance is predicated on a fun- damental tenet of urban ecosystems: humans manage urban areas and, as ultimate ecosystem engineers, can greatly aug- ment or remove resource limitations that favor growth and abundance of some species over others (32, 61). As a result, households with greater discretionary income, capital, higher education, and relaxed pressure for essential needs exert stronger influence on plant assemblages, establishing a resi- dential ecological mosaic based on socioeconomics (32, 50, 62, 65).

The luxury effect is particularly pronounced in arid ecore- gions and biomes, and such effects intensify with increasing urbanization, vegetation loss, and wider wealth gaps (21, 35). Original support for the luxury effect came from Phoenix, Ar- izona, USA, with observed positive correlations between household income and woody perennial diversity (61). Stud- ies investigating the luxury effect globally have implicated wealth as a strong correlate with faunal and floral diversity (26, 63), relative vegetation cover (27, 40), species abundances (49), and the distribution of abiotic attributes in cities includ- ing urban heat islands (35, 66) and environmental hazards (44). Recent meta-analyses have supported the wealth-biodi- versity phenomenon yet emphasized that the causal social and political mechanisms behind these patterns are seldom explored (26, 64). Vegetation cover and biodiversity Affluent urban residential neighborhoods generally have greater vegetation cover, canopy cover, and plant diversity (27, 63, 67). Public urban forests, recreational parks, and pri- vate green spaces also tend to be larger and more established

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with older trees and vegetation that provide greater niche space to support biodiversity at other trophic levels (49, 68, 69). For instance, strong positive correlations exist between urban tree cover and household income for 7 major U.S. met- ropolitan regions (40). General vegetation cover in Los Ange- les, CA (27) and the distribution of urban forests throughout Cook County, Illinois (41) are also positively affected by in- creasing wealth, as well as several other socioeconomic fac- tors (e.g., racial composition, education, home ownership). In addition, recent work suggests interactive effects between housing age and income predict tree biodiversity, with more established homes in high-income neighborhoods exhibiting greater diversity (27). Lawns are a special case where wealth- ier residents intensively manage their lawns to be very green (70) and have few-to-no species other than turfgrasses (71). As a result, some studies find neutral or negative wealth- plant biodiversity relationships (72, 73).

Luxury effects customarily scale from the household to the neighborhood level. A recent study found that yards in wealthier neighborhoods consistently had greater abun- dances and diversity of flowering plants, trees, and nonnative species (65). Similarly, individual homeowners with cost- driven landscaping priorities primarily (i.e., need for cheaper plants) have lawns with higher relative proportions of nonnative plant species with lower functional diversity (50). These recent studies illustrate how socioeconomics drive var- iation among individuals and therefore choices at the house- hold level, which can scale up to affect neighborhood biodiversity. These wealth-driven impacts on patterns of pri- mary producers may have substantial effects on metacommu- nity composition and dynamics. Luxury effects often scale from the residential to the city-wide level, providing cross- city evidence that wealthier U.S. cities have better resourced urban park systems (74). Whether such trends in vegetative structure are consistent across cities, or even hold true across biomes, remains unexplored. Impacts on animal communities Luxury effects extend beyond primary producers, with recent studies suggesting that colonization, species richness, and abundance of birds are related to neighborhood wealth (49, 75–77). Most prior studies address these relationships in birds in multiple cities across the globe. For instance, bird commu- nity richness positively correlates with median household in- come across multiple urban centers in South Africa (49). However, negative income-richness relationships in highly urbanized landscapes imply that highly-built yet expensive downtown centers can deter or prevent successful coloniza- tion and persistence (49). Other studies in Phoenix, Arizona similarly found that bird diversity was greatest in parks and residential yards situated in high-income neighborhoods, a pattern which was primarily explained by an increased

relative abundance of native desert species and proximity to undeveloped desert landscapes (75, 76). Further, recent evi- dence from 45,000 observations of 160 passerine species found across U.S. cities show that increasing household in- come predicts greater abundances of migratory species, as well as greater abundances of smaller, shorter-lived birds (77). These results are some of the first empirical examples linking the luxury effect to evolutionary ecology.

Few studies address the luxury effect in other animal taxa, though evidence implies these effects persist across multiple clades. Evidence in coyotes (Canis latrans) and raccoons (Procyon lotor) throughout Chicago, Illinois suggests carni- vores are more likely to colonize and persist in wealthier neighborhoods (68). Household income is also a strong pre- dictor of lizard species richness in Phoenix, Arizona with other factors like traffic density and surface temperatures having weak effects (78). Evidence from arthropod research suggests that richness in high-income neighborhoods across North Carolina are greater regardless of vegetation cover at the property level (69).

Wealth-animal richness trends can also extend beyond city limits. Red bat (Lasiurus borealis) and evening bat (Nyc- ticeiu humeralis) activity is positively correlated to house- hold income, regardless of land cover metrics (79). Activity patterns of hoary bats (Lasiurus cinereus), however, decrease with neighborhood income, suggesting that luxury effects are more salient for some species relative to others (79). Urban heat islands and air pollution Heat is unevenly distributed within a city, where tempera- tures are typically greatest in lower income compared to higher income neighborhoods (35, 36). Low-income neigh- borhoods have reduced tree and vegetation cover and in- creased impervious surface cover, which contribute to higher surface temperatures in Phoenix, Arizona (35, 66), Baltimore, Maryland (36), as well as other cities worldwide (38, 39, 80). Given the cooling capacity of trees, apparent luxury effects on tree and vegetation cover can significantly impede environ- mental cooling in low-income neighborhoods, making those residents particularly vulnerable to heat-related illnesses (36, 81). Such wealth-tree-heat axes have emerged in other coun- tries as well, including Canada (82), Brazil (83), and South Africa (84, 85). Heterogeneity in the distribution of urban heat islands, and associated health outcomes, is thus a direct consequence of the luxury effect (24, 35).

Other environmental disamenities, especially pollutants, also reflect the luxury effect. Air pollution sources are often co-located near low-income neighborhoods and, conse- quently, low-income residents often have higher risk and vul- nerabilities to air pollutants. For instance, low-income residents throughout North Carolina (44) and multiple cities in the Northeastern U.S. (86) experience greater exposure to

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atmospheric particulate matter. Low-income residents also experience greater ambient nitrogen dioxide concentrations in Montreal, Canada, though some high-income areas in the downtown region similarly experience increased ambient concentrations of this pollutant (87). Further, meta-analysis of data from the American Housing Survey suggests that low- income households have elevated indoor concentrations of nitrogen dioxide and particulate matter (42).

Work on heat islands and pollution support the idea that inequality in neighborhood wealth leads not only to a diver- sity of environmental hazards but that these hazards com- pound to create unique, challenging environmental patches. Limitations of the luxury effect The luxury effect is far from universal across systems and taxa, and the underlying processes and causal mechanisms contributing to emergent wealth-ecology relationships are seldom addressed (21, 40). In a meta-analysis of associations between wealth and biodiversity, the directional relationship (positive, negative, or no relationship) between biodiversity and wealth vary drastically based on differences in social con- ditions, which include cultural norms, individual and com- munity preferences, and municipal policies (26). A pair of similar meta-analyses concluded that relationships between income inequality and urban forest cover are not always sig- nificant, with neighborhood racial composition explaining di- vergent conditions in vegetation cover (64, 88).

The history of urban development, individual-level choices, and societal norms also distort potential relation- ships between wealth and biodiversity. For instance, in some cities, wealthier neighborhoods may have a higher relative proportion of high rises and built downtowns that severely limit the amount of vegetated cover, reducing functional hab- itat space and biodiversity (26). Wealthier neighborhoods may also enact policies that reduce vegetation diversity and mandate the proliferation of monoculture lawns that yield significant environmental homogeneity and serve to similarly reduce biodiversity (26). Moreover, refined analytical ap- proaches may help to disentangle the contribution of wealth, culture, and other socioeconomic factors to ecology. For ex- ample, evidence in New York City suggests residential canopy cover is best explained as a signal of social status (the “ecol- ogy-of-prestige hypothesis”) (32). Hence, the convergence among policy, individual choices, and socioeconomic varia- bles might be better predictors of urban ecological variance rather than wealth alone (32). Indeed, recent work assessing the plant diversity of residential yards supports this conclu- sion, suggesting that individual homeowner’s landscaping priorities largely dictate private lawn community composi- tion (50).

Luxury effects have been primarily explored in terrestrial systems, with less work in aquatic habitats. Lack of evidence

for aquatic luxury effects in urban ponds, lakes, and rivers may be due to other abiotic factors regulating waterway health that do not necessarily correlate with wealth dispari- ties (63). Small ponds or lakes are also seldom present in lower socioeconomic areas, functionally eliminating poten- tial studies on aquatic luxury effects. Moreover, riverfront or coastal environments have increasingly become hotspots for the wealthy, excluding lower-income communities and thereby compounding ostensible luxury effects. Urban rivers and streams run through and interconnect high- and low-in- come areas, so downstream habitats may suffer consequences of upstream pollution and erosion.

Characteristically, the luxury effect has also resided at the community and ecosystem level, with few studies investigat- ing how wealth heterogeneity impacts organismal and popu- lation ecology (68, 79). Prior studies also predominantly address patterns but seldom articulate the underlying socio- political processes that contribute to wealth-ecology relation- ships. Integrating systemic racism and environmental justice should emerge as the next development in socio-ecological scholarship. Beyond wealth: Structural racism, ecology, and evolution In multiple cases, neighborhood racial composition can be a stronger predictor of urban socio-ecological patterns than wealth (25, 37, 88). For example, exposure to particulate mat- ter in cities like Los Angeles (43), Phoenix (46), and through- out the state of North Carolina (44), is increased for racial and ethnic minority groups, especially Black, Latinx (i.e., a person of Latin American origin), and Native American pop- ulations (43, 45). The geographic distribution of urban heat islands and tree canopy cover in cities is also stratified by race: multiple studies have repeatedly demonstrated that land surface temperatures are magnified for racially minori- tized groups in many U.S. cities (36, 37, 39), with certain ra- cial groups more vulnerable than others (37, 38). Differential pollutant exposure extends to aquatic systems. For example, decades of neglected pollution in the Flint River, Michigan, led to an ecological disaster for the stream biota and a mas- sive ongoing humanitarian crisis (47, 48). Pressures to save money motivated the local government to switch the predom- inantly Black community of Flint’s source of drinking water from Lake Huron to the polluted river (89). The calamity of the polluted Flint drinking water is just one example of a larger pattern for minoritized communities bearing the brunt of ecosystem disamenities (48).

Recent studies have begun to reveal some of the underly- ing structural constructs, especially racism, that contribute to urban heterogeneity beyond household income (28, 37, 88). However, determining the true influence systemic and struc- tural racism exerts on ecological dynamics remains a novel

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area of investigation (28). Studies on the resultant evolution- ary outcomes are also rare (90). Knowing the relative contri- bution of structural racism to wealth disparities informs our understanding of complex temporal dynamics in cities, which is untenable in approaches lacking historical contexts (21, 24). In addition, incorporating structural racism into biolog- ical models should improve their predictive value thereby al- lowing us to better estimate the true effect of urbanization on evolutionary and ecological change. Frameworks that consider systemic and structural racism as principal drivers of urban form advance our ability to predict how and which species may acclimatize and evolve for life in cities (Figs. 2 and 3). Residential segregation and redlining Globally, residential segregation is an especially potent form of social stratification, characterized by a physical separation of groups within cities and further compounded by the con- centration of government and ecosystem benefits (30). Criti- cally, residential segregation shapes ecological conditions along multiple environmental axes that cannot be neatly characterized by variables such as wealth or impervious sur- face cover (91). This is particularly important because social geographies vary for different racial, ethnic, and cultural groups depending on the varying historical forms of discrim- ination experienced by each minoritized group (31). The im- pact of structural racism on Black geographies in the U.S. have been particularly well documented, with profound leg- acy effects on urban ecological patterns (21, 24, 27, 92).

Perhaps one of the most notorious examples of structural racism is the U.S. sanctioned policy of “redlining” enacted be- tween 1933–1968. This policy segregated urban residential neighborhoods principally by race and was used to formally suppress capital wealth gains of Black Americans (30). Red- lining graded neighborhoods from most desirable (“A”, out- lined in green) to hazardous (“D”, outlined in red) based on the perceived amenities and disamenities including financial riskiness, environmental quality, proximity to industrial fa- cilities, and racial composition of the neighborhood (Fig. 2) (30). Black Americans were refused housing loans and walkthroughs in neighborhoods deemed “A” or “B” quality and relegated to “C” and “D” areas that received less govern- mental support.

Today, the ecological effects of redlining persist. Redlined “D” neighborhoods have on average 21 percent less tree can- opy than “A” neighborhoods. Further, “A” graded areas are frequently more uniformly green, have older tree canopy, are closer to environmental amenities than redlined “D” neigh- borhoods (Fig. 2). Though no longer a policy, studies have shown that the legacy of redlining remains a key driver of contemporary urban landscapes across at least 37 cities in the United States (24, 28, 92).

Ecological effects of structural racism Redlining may greatly contribute to the asymmetric distribu- tion of habitat that structures bottom-up processes influenc- ing biodiversity (28, 35). Reductions in tree and vegetation cover necessarily diminish niche diversity and quality (63, 93), which frequently coincides with reduced species richness of birds, mammals, and arthropods (94–97). By concentrating Black Americans and other minoritized communities in ur- ban centers, redlining often reduced the proximity of segre- gated areas to undeveloped landscape beyond the urban boundary (Fig. 2A) and patterns of segregation may have sub- sequently created variably permeable urban matrices (Fig. 2B). Therefore, we may hypothesize that emergent patterns of species colonization and extinction vary considerably within and among cities as a function of heterogeneous tem- poral and spatial legacies of racial segregation. A critical question is whether the severity and age of residential segre- gation impacts the number of species co-occurring at a local- ized site (alpha diversity), a reduction in community composition across sites over space and time (beta diversity), or city-wide regional biodiversity (Fig. 3 and Table 1).

Archived redlined maps may prove valuable for predicting the spatial distribution of niches across cities (Fig. 2). Be- cause redlining predicts the age, abundance, and distribution of urban tree canopy in many cities, it is likely that such maps may also provide substantial resolution to the geographic lo- cations of potential sink habitats and ecological traps in both terrestrial and aquatic environments (98). Though several studies have addressed the emergence of source and sink habitats (99–102), none have explicitly considered whether heterogeneity in pollutants, heat, and other disturbances shape their geographic distribution (i.e., Fig. 1A). The legacy effects of residential segregation could predict the locality and size of potential ecological sinks and traps, thereby help- ing to identify and predict geographic regions with com- pounding anthropogenic disturbances that require more sustained stewardship (Table 1).

Recent studies emphasize that the spatial arrangement of vegetation cover can drive evolutionary change (103), funda- mentally linking segregation-driven patterns of vegetation cover to shaping evolutionary trajectories of urban popula- tions. Impervious surface is frequently associated with re- duced movement of organisms across landscapes and therefore lower gene flow, more subdivided populations, and lower genetic diversity (104–106). Urban

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