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Bioscience Article Overview Articles The Biological Deserts Fallacy: Cities in Their Landscapes Contribute More than We Think to Regional Biodiversity Downloaded from https://academic.oup.com/bioscience/article/71/2/148/6102678 by guest on 17 February 2021 ERICA N. SPOTSWOOD , ERIN E. BELLER, ROBIN GROSSINGER, J. LETITIA GRENIER, NICOLE E. HELLER, AND MYLA F. J. ARONSON Cities are both embedded within and ecologically linked to their surrounding landscapes. Although urbanization poses a substantial threat to biodiversity, cities also support many species, some of which have larger populations, faster growth rates, and higher productivity in cities than outside of them. Despite this fact, surprisingly little attention has been paid to the potentially beneficial links between cities and their surroundings. We identify five pathways by which cities can benefit regional ecosystems by releasing species from threats in the larger landscape, increasing regional habitat heterogeneity and genetic diversity, acting as migratory stopovers, preadapting species to climate change, and enhancing public engagement and environmental stewardship. Increasing recognition of these pathways could help cities identify effective strategies for supporting regional biodiversity conservation and could provide a science-based platform for incorporating biodiversity alongside other urban greening goals. Keywords: biodiversity conservation, urban biodiversity, cities, regional ecosystems, habitat heterogeneity ities are embedded in and connected to their of ecological roles cities play within their landscapes and Csurrounding landscapes. Energy, resources, and spe- of how positive roles can be bolstered through intentional cies all flow across political and geographic boundaries, design. Filling this gap can guide the design and manage- with impacts on landscape-scale biodiversity. Although ment of urban green spaces to enhance their contributions urbanization poses a substantial threat to biodiversity to regional and global biodiversity conservation. Over the (McDonald et al. 2020), cities also support many species, coming decades, as urban footprints grow and the impact some of which have larger populations, faster growth rates, of climate change on biodiversity accelerates, we will need and higher productivity in cities than elsewhere (Faeth cities to contribute to and support global biodiversity et al. 2011, Bateman and Fleming 2012). Despite this fact, conservation. discussion of the implications of ecological links between Cities are unique features, often differing markedly from cities and their surrounding landscapes has focused pri- their surrounding landscapes. They are often located in marily on the negative impacts, including the export nonrandom settings with distinctive topographic, edaphic, of pollution (Grimm et al. 2008b, Hien et al. 2020) and and hydrologic characteristics, resulting in underlying dif- invasive species (Aronson et al. 2007, Von der Lippe and ferences between cities and their surroundings irrespective Kowarik 2008, Bar-Massada et al. 2014, Padayachee et al. of urbanization (Luck 2007). Urbanization further modifies 2017), the impacts of domesticated animals on wildlife the physical landscape and climate, intensifying differences in adjacent wildland areas (Lepczyk et al. 2004, Metsers between cities and their surroundings (Grimm et al. 2008b, et al. 2010, Hanmer et al. 2017), and the potential of cities Pickett et al. 2011, Kaushal et al. 2014). Plant and animal to create ecological traps (Battin 2004, Sumasgutner et al. communities are also altered: cities tend to have higher 2014, Spear et al. 2018, Tella et al. 2020). However, the numbers of nonnative species and are often dominated by successes of some native, nonpest species in cities suggests urbanization-tolerant or synanthropic species (Faeth et al. that we have an incomplete understanding of the full suite 2011). Resulting novel species assemblages alter trophic BioScience 71: 148–160. © The Author(s) 2021. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. doi:10.1093/biosci/biaa155 Advance Access publication 20 January 2021 148 BioScience • February 2021 / Vol. 71 No. 2 https://academic.oup.com/bioscience 148-160-biaa155.indd 148 05-02-2021 07:30:33 PM Overview Articles structures and phenologies, which can reduce available historically allowed people to take advantage of temperate resources. climates, rich agricultural soil, and navigational opportuni- Landscapes surrounding cities also vary widely from ties (Kühn et al. 2004). As a result, more people live at lower relatively intact ecosystems to ecosystems highly modi- elevations and within 100 kilometers of a shoreline than fied by intensive or extensive agriculture and plantation expected by chance (Luck 2007), and soil, topography, avail- forests (Grimm et al. 2008a, Oliveira Hagen et al. 2017). ability of freshwater, climate, and solar radiation all play a Surrounding landscapes also vary in habitat quality and role in where contemporary cities are located (Kühn et al. resource availability depending on the degree of distur- 2004). The same factors that draw people to these areas bance and habitat homogeneity (Oliveira Hagen et al. 2017, also tend to support other taxa, and many cities have been Phillips et al. 2018). Where surrounding landscapes pro- built in biodiversity hotspots and in locations with high vide high-quality and diverse habitats, there may be little net primary productivity (Luck 2007). The result can lead advantage for species to venture into cities. In other cases, to strong environmental gradients between cities and their Downloaded from https://academic.oup.com/bioscience/article/71/2/148/6102678 by guest on 17 February 2021 extreme disturbance in the surrounding landscape may lead surrounding landscapes in geology, topography, elevation, to more resources and opportunities in cities compared with and hydrology that are unrelated to human modification or their surroundings. These differences, combined with varia- urbanization (figure 1). tion in how species respond to urbanization, lead to large Urbanization also alters abiotic and biotic conditions, cre- differences in how species use urban landscapes, and what ating gradients between cities and their surrounding land- benefits cities may provide. scapes in hydrology, air temperature, atmospheric chemistry, The unique conditions found in cities have a variety of and climate (Grimm et al. 2008a, Pickett et al. 2011, Kaushal species-specific impacts that range from negative to neutral et al. 2014). For example, the urban heat island effect to positive depending on each species’ behavioral and life- increases mean growing season lengths and shifts phenol- history characteristics and tolerance to urbanization (Evans ogy in many plant species, leading to earlier and longer et al. 2011, Sol et al. 2014). Although overwhelming evidence flowering seasons than in rural areas (Harrison and Winfree suggests that urbanization is a net negative for biodiversity, 2015, Leong et al. 2016). In addition, resources and nutrient there are also many informative examples of species that are availability are often altered in cities because of the presence either neutrally effected or doing well in cities. For example, of human food (including supplemental feeding and food unique habitat features in cities may support particular spe- waste) and differences in net primary productivity. cies or life history needs, or provide refuge from threats in Differences between cities and their surrounding land- the surrounding landscape. In addition, there is potential for scapes also depend on what type of land use surrounds a cities to both increase regional genetic diversity and create city. Although relatively intact habitat is found around some populations that are better able to tolerate future conditions cities, many are surrounded by highly modified landscapes, under climate change (Johnson and Munshi-South 2017). either through intensive or extensive agriculture or planta- Here, we identify potential positive impacts of cities on tion forests. How cities compare with their surroundings is regional ecosystems. We acknowledge the well established highly context dependent, given that both cities and their and overall negative consequences of cities on biodiversity surroundings vary globally in the degree of human distur- (McDonald et al. 2020). We focus on highlighting specific bance and extent of modification. For example, in a recent ways that cities support plant and animal species while analysis across three continents, cities with more vegeta- also examining the many negative impacts of urbanization. tion showed less of a difference in the functional diversity First, we discuss what makes urban landscapes unique in a of avian assemblages compared with their surroundings landscape context and the species-specific implications of (Oliveira Hagen et al. 2017). Resource availability and the unique conditions found in cities. We then propose five habitat quality can also change over time as cities age and pathways by which cities can contribute positively to their as human behavior and preferences shift, leading to shifts regions, including providing release
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