Impact Factor 2.686 | CiteScore 2.51
More on impact ›

Perspective ARTICLE

Front. Ecol. Evol., 21 June 2019 | https://doi.org/10.3389/fevo.2019.00220

Does Nature Need Cities? Pollinators Reveal a Role for Cities in Wildlife Conservation

Abigail Derby Lewis1*, Mark J. Bouman1, Alexis M. Winter1, Erika A. Hasle1, Douglas F. Stotz1, Mark K. Johnston1, Karen R. Klinger1, Amy Rosenthal1 and Craig A. Czarnecki2
  • 1Keller Science Action Center, Field Museum, Chicago, IL, United States
  • 2United States Fish and Wildlife Service, Minneapolis, MN, United States

It is well-established that cities need nature for critical ecosystem services—from storing carbon, to reducing temperatures, to mitigating stormwater—and there is growing momentum to seek out strategies for how these services can intersect with urban design and planning efforts. Social scientists and conservation planners increasingly point to urban residents' need to breathe fresh air, encounter the natural world, and have room to play. It is less obvious, perhaps, whether nature needs cities in order to thrive. The evidence from both urban planning and conservation planning is increasingly “yes.” As changes in land use and land cover sweep the planet, cities are becoming important refugia for certain wildlife populations. In recent years, urban planning has embraced the concept of “green infrastructure” as a way to embed green space across metropolitan landscapes to draw on the inherent benefits nature provides to cities, as well as to create habitat for wildlife. We explore this evolving view of cities and nature in the fields of urban and conservation planning. We argue the time is ripe to bring these worlds together, and, using our empirical work, establish that cities matter for monarch butterflies, other pollinators, and at-risk wildlife species.

Why focus conservation efforts in cities?

More than 80% of Americans live in urban areas1, as does over half the world's population (UN DESA, 2018). In contrast, in 1960 twice as many people in the world lived in rural areas (2 billion) as urban (1 billion)2. This trend is expected to continue, with nearly 70% of the world's population living in urban areas by 2050 (UN DESA, 2018). However, a striking 60% of the additional land projected to become urban by 2030 is yet to be built (GFDRR World Bank, 2015). Each day in the US more than 4,000 acres of open space are lost to development, the equivalent of more than three acres per minute (Williams, 1975).

As changes in land use and land cover sweep the planet, converting grasslands, forests, wetlands, and other available habitat into agricultural fields and developed landscapes, cities are becoming increasingly important refugia for an array of wildlife populations, including threatened and endangered species (Aronson et al., 2014; Ives et al., 2016). This pattern reflects, in part, the propensity to locate urban development in biologically diverse areas such as coastal and riparian locations (Luck, 2007). Indeed, populations of many species are reappearing in force across urban spaces—from fishers (LaPoint et al., 2015) and coyotes (Morey et al., 2007) to bullfinches (Audet et al., 2016) and peregrines (Caballero et al., 2016). Other urban wildlife dwellers include migratory species of birds, dragonflies and butterflies that rely on habitat patches in cities to move through landscapes dominated by large-scale agriculture (Seewagen et al., 2011; Goertzen and Suhling, 2013; Tam and Bonebrake, 2016). Significantly, several American cities support a higher diversity of native bee species—including the endangered rusty patched bumble bee (Bombus affinis)—than do adjacent rural areas (Hall et al., 2017; U.S. Fish Wildlife Service, 2017). These examples of wildlife species utilizing urban habitat illustrate that developed areas can be important in the conservation of species of high concern.

Given these trends, we have a small but critical window of time to develop and implement strategies that create highly functional urban landscapes with benefits for both people and nature (Intergovernmental Science-Policy Platform on Biodiversity Ecosystem Services (IPBES), 2019). Understanding how habitat can best be embedded in urban landscapes is important to help curb a potential “sixth mass extinction” (Ceballos et al., 2015, 2017). This situation cannot be overstated: recent studies reveal that the number of mammals, birds, fish and reptiles on Earth has been reduced by 60% in <50 years (World Wildlife Fund, 2018). In Germany, flying insect populations have plunged by 75% in the last 25 years (Hallmann et al., 2017), and a similar trend has been observed in Puerto Rico (Lister and Garcia, 2018).

Powerful urbanization trends have understandably been accompanied by a sense that nature has been displaced in urban landscapes and can only be found where cities don't exist (Hartig and Kahn, 2016). On the one hand, urban life has been characterized as “distanced from nature” (Tuan, 1978) accompanied by an “extinction of experience” (Pyle, 1978, 1993) as people move to urban settings (Miller and Hobbs, 2002; Turner et al., 2004; Zhang et al., 2014; Soga and Gaston, 2016). On the other hand, the conservation community has achieved huge victories in places far from the urban world, and a side effect has been to reify the notion of “wilderness” in the American mind (Nash, 1967). Large protected areas have “increasingly become the means by which many people see, understand, experience, and use the parts of the world that are often called nature and the environment” (West et al., 2006, p. 255).

As we'll discuss, our work on monarch conservation surfaces new ways to bring the potential for urban conservation into sharper focus. This new way of “seeing” cities includes: valuing new potential partners for nature, many of them historically excluded from the conservation narrative (Finney, 2014; Taylor, 2016); applying finer scales of analysis, with the aid of new data and geospatial tools; and recognizing other practices now being adopted to create sustainable cities for people. A main takeaway from our research is that the places called “urban”—in all their size, density, and heterogeneity (Wirth, 1938)—do contain powerful voices, activities, and opportunities for conservation. In spite of the perception that racial minorities and low-income Americans—who are often well-represented in urban regions—are considered to have little concern for nature, a recent study reports their higher concern for nature than white and higher-income respondents (Pearson et al., 2018). Activating that concern for conservation may entail folding “nature” into the broader set of priorities that residents and community-based organizations have.

From backyards to rooftops to parks, urban residents have seen to it that nature has a place in the city, from the ground up. Improvements in technology have made this activity increasingly visible from the sky down. Wherever possible, our monarch research employed high-resolution imagery, enhanced by technology such as LiDAR3, which enabled precise characterization of land cover at the sub-meter scale. This helps us to visualize what is happening in the urban area with greater precision than the commonly used National Land Cover Database (NLCD), a 30-meter resolution dataset most appropriate to use when studying county-level units or larger (Wickman et al., 2014). When NLCD is applied to highly heterogeneous metropolitan landscapes, large swaths of land are classified as high, medium and low intensity developed land cover classes. While “low intensity developed” and “medium intensity developed” indicate a moderate proportion (20–79%) of the land cover is impervious, higher resolution data are needed to quantify and visualize the remaining land that is permeable and usable as green space. Figure 1 demonstrates a sample area in Chicago's urban core viewed using NLCD, aerial imagery with LiDAR, and plantable space. Finer grain analysis can support the growing recognition that cities are ripe with opportunity and interest to create spaces where both people and wildlife benefit (Rosenzweig, 2003). This new perspective helps us to appreciate nature abounding in a multitude of contexts that intersect with how people live, work and play in urban areas, including in churchyards and school yards, along boulevards, and amidst corporate campuses, residential yards and community gardens (Beatley, 2011; Van Horn and Aftandilian, 2015;Johnston et al., 2019).

FIGURE 1
www.frontiersin.org

Figure 1. Comparison of land cover data as classified when applying (A) the National Land Cover Dataset derived from 30-m spatial resolution Landsat satellite data, (B) higher spatial resolution land cover data derived using 2-foot spatial resolution multispectral aerial imagery and LiDAR data, and (C) grass-shrub land cover class in isolation (i.e., plantable space). This scale reveals the many opportunities that exist even under highly developed conditions. Sources: Multi-Resolution Land Characteristics Consortium (U.S.). “National Land Cover Dataset (NLCD)” and University of Vermont Spatial Analysis Lab “Chicago Urban Tree Canopy.”

Much of what can be seen, and what exists as an opportunity to enhance urban biodiversity going forward, comes in the context of burgeoning “green infrastructure” efforts (Benedict and McMahon, 2006; Hostetler et al., 2011; Ahern, 2013). The uptick of interest in green infrastructure relates to how well it supports a number of needs in urban areas, including: enforcement efforts to bring municipalities into compliance with the pollution control provisions of the federal Clean Water Act4; nature-based solutions to reduce climate impacts such as flooding in urban landscapes (Derby Lewis et al., 2015); public interest in native landscaping (McMahan, 2006); the growing sector of urban farming (Jarosz, 2008; Lovell, 2010); and increased access to nature, particularly in marginalized neighborhoods (Wolch et al., 2014).

We propose that pollinator-focused efforts can help to find alignment between conservation goals and concerns important to cities and urban dwellers. Pollinators are small organisms that interact with households and neighborhoods, but operate in the larger landscape scale—and their associated habitats can leverage a variety of design and management activities that are underway in cities and offer pathways to connect nature and cultural heritage in urban communities. In short, monarchs (and other pollinators) point to new ways to “see” the city as a space for conservation, with new partners, new tools, and new practices.

How can the monarch butterfly help us to understand the role cities can play in conservation?

While many pollinators in general have wide public appeal, the monarch butterfly (Danaus plexippus) is arguably an ideal ambassador to engage the public on conservation issues. Monarchs are an iconic animal with a well-known migration and striking orange and black coloration. They also represent a powerful cultural symbol that facilitates people talking about conservation—and to one another (Gustafsson et al., 2015). Monarchs have been referred to as a convener: a species able to connect people across a continent who witness the stunning migration in their own backyard. Currently, there is heightened public awareness that monarchs, like many pollinators locally and globally, are declining rapidly. Over the last two decades, the eastern monarch population has decreased by more than 80% (Semmens et al., 2016), while the western population has declined by a staggering 97% (Schultz et al., 2017). The public interest in monarchs and a growing awareness of their plight create an opportunity to translate attitudes into practices that can help a range of pollinators across the urban landscape. Through our efforts and those of others, we are beginning to discover how monarchs are relevant to the future of conservation, as well as different entry points—from social justice and cultural history to sustainable food initiatives—for engaging people in creating urban habitat (Gustafsson et al., 2015; Derby Lewis et al., 2018).

A Monarch's View of the City

A combination of efforts such as the creation of a Federal Strategy to Promote the Health of Pollinators5 and an assessment to determine whether monarchs need Endangered Species Act protection6, along with a variety of current urban monarch initiatives (e.g., Mayors' Monarch Pledge7 and Monarch Watch8), led the U.S. Fish and Wildlife Service and the Field Museum in Chicago to collaborate in assessing the role cities could play in helping to increase the amount of habitat available to support eastern monarch butterflies. While this research does not apply to the Western monarch population, whose numbers have declined so dramatically (Schultz et al., 2017) that individuals are not frequently observed in the urban landscape, lessons can be drawn to support broader pollinator habitat efforts in metropolitan landscapes throughout the United States.

The aim of this effort was (1) to evaluate how much the urban sector, which is the second largest land use sector in the eastern monarch's Midwestern breeding range (Thogmartin et al., 2017), could contribute to the national goal of adding 1.8 billion milkweed stems (Semmens et al., 2016) and (2) to identify best practices for engaging a diversity of urban stakeholders in the creation of monarch habitat. Our team of ecological and social scientists then translated this information into a suite of spatial and social planning tools to help decision makers identify where the biggest opportunities exist to increase monarch habitat, and guidance on how to turn potential into reality. Details of the methods used to estimate the number of existing and potential milkweed stems occurring in urban landscapes, and to identify strategies to engage stakeholder groups to create habitat, have been published elsewhere (Johnston et al., 2019). For the purposes of this perspective, we provide a high-level summary of the approach and key findings, and discuss implications of this work in a broader context.

To understand the ecological landscape from a monarch's perspective, we conducted field sampling to estimate how much milkweed is currently on the ground and quantified the potential space for planting additional monarch habitat (i.e., the amount of grass/shrub land cover identified using high-resolution imagery and LiDAR data9) in different land use classes within four major metropolitan regions: St. Paul-Minneapolis, Chicago, Kansas City and Austin. For comparison purposes, land use types were consolidated into 16 classes based on land management (e.g., residential-single family, community and cultural, open space conservation, etc.). Milkweed stems were counted in three ways: (1) randomly sampled census blocks located at staggered distances along transects extending through the metropolitan area, (2) targeted sampling of open space conservation and non-conservation areas, and (3) targeted sampling of locations where milkweed was intentionally planted. Based on the density of milkweed present in each of the land use classes, we extrapolated the amount of milkweed that is currently present and the potential to add additional milkweed stems in metropolitan areas across the US eastern range of monarchs. Our findings indicate the collective impact of this potential contribution could provide nearly a third of the additional 1.8 billion milkweed stems needed in the Midwest to stabilize the eastern monarch's population (Johnston et al., 2019).

Additionally, we looked at the potential plantable space across each land use class to provide a more detailed characterization of the urban landscape. For example, in the Chicago region, we found that residential land had one of the highest amounts of potential plantable space. Using a land use lens allowed us to link high-potential areas with the stakeholders that would need to be engaged to increase monarch habitat. We were then able to pair those stakeholders with evidence-based approaches to enhance uptake (Figure 2).

FIGURE 2
www.frontiersin.org

Figure 2. This figure shows how the geospatial and social tools may be used together to plan urban monarch conservation in a strategic way. In this example, residential land has been identified as an area with a large amount of plantable space that could become monarch habitat. The city of Chicago (or an organization active in the city) might target residential land for habitat improvement, using approaches appropriate to residential stakeholders as described by the team's social scientists in the Urban Monarch Conservation Guidebook10.

To identify appropriate approaches for different stakeholder groups in an urban setting, we conducted social science research to assess the motivations, concerns, interests, challenges, and strategies of those both directly and indirectly involved in making their city's landscape more hospitable to monarchs. We surveyed people engaged in different environmental practices (e.g., planting/managing land, designing landscapes, monitoring the natural environment) and within the different land use classes laid out by the team's geospatial analysts. With people who had extensive knowledge or experience relevant to monarch conservation, we conducted semi-structured interviews, as they make efficient use of the participant's time and are well-suited to the exploratory phase of research (Schensul and LeCompte, 2013). For participants drawn from the “interested public,” we used an online survey, which allowed us to reach more people. We collected and analyzed 734 online surveys and 75 semi-structured interviews in the four pilot metropolitan areas and found that interest in creating monarch habitat was present to varying degrees across all groups, but it took different forms. For example, while some stakeholder groups are singularly focused on the monarch, others may be more interested in broader habitat creation and/or wary of the regulations that single-species conservation can bring. This information was used to highlight best practices for engaging urban stakeholders and to develop approaches that connect to community interests and assets (e.g., social justice initiatives, green infrastructure planning, urban farming efforts, public art) in engaging a wide cross-section of urban residents to take actions aligned with wildlife conservation goals.

Does Nature Need Cities?

Our results add to a growing body of literature showing that metropolitan areas matter for wildlife conservation (Morey et al., 2007; LaPoint et al., 2015; Caballero et al., 2016). Despite being developed, these landscapes have high potential to maintain functional habitat for a variety of species, including migratory and threatened endemic species. Habitat within and between US cities can help connect the dots for monarchs, other pollinators, and birds along migratory pathways from Mexico to Canada and back.

The importance of cities for maintaining insect pollinators is particularly noticeable, given the relatively small spatial and temporal requirements for functional pollinator habitat that can be satisfied in urban green spaces. Although urban habitats are highly heterogeneous, with habitat often occurring in isolated patches, evidence suggests there is sufficient opportunity for pollinators to use these spaces (Tommasi et al., 2004; Glaum et al., 2017; Hall et al., 2017)—sometimes even greater opportunity than in surrounding rural areas.

As is the case with any land use sector, however, there are considerations that need to be addressed. For example, the wide-scale use of pesticide and herbicide in urban landscapes (Hladik and Kolpin, 2015) by public entities and private landowners poses a threat to insect population health. To ensure a net gain for pollinator populations utilizing urban habitat, approaches that limit insecticide exposure in urban areas are recommended.

Interdisciplinary methods that bring together the insights of social, natural and spatial sciences can shed light on the conservation approaches with the most ecological and social potential to scale effective solutions. Our work suggests that the collective impact of conservation-related actions by urban stakeholder groups can play a fundamental role in supporting wildlife—including nearly a third of the milkweed needed for the eastern monarch (Johnston et al., 2019). By identifying the ecological potential and understanding the social perspectives and interests of different stakeholder groups, it is possible to enhance the uptake of conservation strategies within urban areas, where these practices are important for threatened species.

Metropolitan areas also offer the opportunity to engage millions of people in conservation efforts. Despite urban areas' representing only 3% of the total landmass in the US, these areas have a disproportionate influence on the landscape, and investments must be made to turn the urban conservation potential into a reality. Expanding the functional habitat within these urban centers and increasing the commitment of urban stakeholder groups to conservation goals could greatly contribute to the achievement of those goals.

This means we must identify the different entry points where conservation goals can include input from urban partners and overlap with community values and concerns. Embracing community values as assets in conservation planning creates more opportunity for habitat and fosters meaningful new partnerships that are essential in highlighting conservation relevance in a rapidly expanding urban world.

A broader vision of what conservation is, what nature looks like beyond protected lands, and who is included in the conservation community is long overdue. Acknowledging that there are different ways that heritage and history shape how people experience the natural world, or see nature as a part of their lives, is an important first step in broadening the conservation community (Campbell, 2015). Our research indicates that cities can play a critical role in species and habitat conservation and that interdisciplinary approaches that engage urban stakeholders can have an outsize impact on wildlife conservation.

Author Contributions

ADL, MB, AW, EH, DS, MJ, and CZ contributed to the conception of the design and the study. ADL wrote the first draft of the manuscript. ADL, MB, and AW wrote sections of the manuscript. All authors contributed to manuscript revision, read, and approved the submitted version.

Funding

A cooperative agreement between the United States Fish and Wildlife Service, Chicago Wilderness, and the Field Museum. Grant Award number CW FMNH 103115. Publication fees for open access were paid for by the Field Museum.

Disclaimer

The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

We would like to thank the deeply committed and creative team of individuals whose work is reflected in this study, including Tim Bodeen, Katie Boyer, Brittany Buckles, Wendy Caldwell, Louise Clemency, Jill Erickson, Caitlin Dix, Ryan Drum, Nigel Golden, Adriana Fernandez, Jessica Hellman, Kyle Kasten, Marc Lambruschi, Laura Lukens, Cora Lund-Preston, Patrick Martin, Katie Maxwell, Tom Melius, Kelley Myers, Rosie Nguyen, Karen Oberhauser, John Rogner, Jason Rowader, Glen Salmon, Kristin Shaw, Wayne Thogmartin, Chuck Traxler, Kristin Voorhies, Gwen White, and Barbara Willy. We also thank Debra Moskovits, Ellen Woodward, Iza Redlinski, and Jacob Campbell for their review and comments on this paper.

Footnotes

1. ^U.S. Census Bureau. (2010). Available online at: https://www.census.gov/geo/reference/ua/urban-rural-2010.html

2. ^Our World in Data. Available online at: https://ourworldindata.org/urbanization

3. ^LIDAR, or Light Detection and Ranging, is a “remote sensing method that uses light in the form of a pulsed laser to measure ranges (variable distances) to the Earth.” Available online at: https://oceanservice.noaa.gov/facts/lidar.html

4. ^Technical Report: Tools, Strategies and Lessons Learned from EPA Green Infrastructure Technical Assistance Projects. Available online at: https://www.epa.gov/green-infrastructure/tools-strategies-and-lessons-learned-epa-green-infrastructure-technical

5. ^Pollinator Partnership Action Plan. Available online at: https://www.whitehouse.gov/sites/whitehouse.gov/files/images/Blog/PPAP_2016.pdf

6. ^Assessing the Status of the Monarch Butterfly. Available online at: https://www.fws.gov/savethemonarch/SSA.html

7. ^Mayors' Monarch Pledge is a program designed to support U.S. cities, municipalities, and other communities committing to create habitat for the monarchs and other pollinators. Available online at: https://www.nwf.org/Garden-For-Wildlife/About/National-Initiatives/Mayors-Monarch-Pledge.aspx

8. ^Monarch Watch is “a nonprofit education, conservation, and research program based at the University of Kansas”. Available online at: https://monarchwatch.org/

9. ^Urban Tree Canopy Assessment. Available online at: https://www.nrs.fs.fed.us/urban/utc/

10. ^www.fieldmuseum.org/monarchs

References

Ahern, J. (2013). Urban landscape sustainability and resilience: the promise and challenges of integrating ecology with urban planning and design. Landscape Ecol. 28, 1203–1212. doi: 10.1007/s10980-012-9799-z

CrossRef Full Text | Google Scholar

Aronson, M. F. J., La Sorte, F. A., Nilon, C. H., Katti, M., Goddard, M. A., Lepczyk, C. A., et al. (2014). A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc. R. Soc. B Biol. Sci. 281:330. doi: 10.1098/rspb.2013.3330

PubMed Abstract | CrossRef Full Text | Google Scholar

Audet, J., Ducatez, S., and Lefebvre, L. (2016). The town bird and the country bird: problem solving and immunocompetence vary with urbanization. Behav. Ecol. 27, 637–644. doi: 10.1093/beheco/arv201

CrossRef Full Text | Google Scholar

Beatley, T. (2011). Biophilic Cities: Integrating Nature into Urban Design and Planning. Washington, DC: Island Press.

Google Scholar

Benedict, M. E., and McMahon, E. T. (2006). Green Infrastructure: Linking Landscapes and Communities. Washington, DC: Island Press.

Google Scholar

Caballero, I. C., Bates, J. M., Hennen, M., and Ashley, M. V. (2016). Sex in the city: breeding behavior of urban peregrine falcons in the Midwestern US. PLoS ONE 11:e0159054. doi: 10.1371/journal.pone.0159054

PubMed Abstract | CrossRef Full Text | Google Scholar

Campbell, J. (2015). Placemaking with Culture and Nature on Chicago's South Lakefront. Pract. Anthrol. 37, 35–36. doi: 10.17730/0888-4552-37.3.35

CrossRef Full Text | Google Scholar

Ceballos, G., Ehrlich, P. R., Barnosky, A. D., García, A., Pringle, R. M., and Palmer, T. M. (2015). Accelerated modern human–induced species losses: entering the sixth mass extinction. Sci. Adv. 1:5. doi: 10.1126/sciadv.1400253

PubMed Abstract | CrossRef Full Text | Google Scholar

Ceballos, G., Ehrlich, P. R., and Dirzo, R. (2017). Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. PNAS J. 114:E6089. doi: 10.1073/pnas.1704949114

PubMed Abstract | CrossRef Full Text | Google Scholar

Derby Lewis, A., Moseley, R. K., Hall, K. R., and Hellmann, J. J. (2015). “Conservation of urban biodiversity under climate change: climate-smart management for chicago green spaces,” in Handbook of Climate Change Adaptation, ed W. Leal Filho (Berlin: Springer), 277–296. doi: 10.1007/978-3-642-38670-1_11

CrossRef Full Text | Google Scholar

Derby Lewis, A., Winter, A., Czarnecki, C., and Bouman, M. (2018). “Connecting nature and society to increase conservation relevance: a case study of the monarch butterfly in urban areas,” in Transactions of the 82nd North American Wildlife and Natural Resources Conference (Spokane, WA: Wildlife Management Institute).

Google Scholar

Finney, C. (2014). Black Faces, White Spaces: Reimagining the Relationship of African Americans to the Great Outdoors. Chapel Hill: The University of North Carolina Press.

Google Scholar

GFDRR and World Bank (2015). Investing in Urban Resilience: Protecting and Promoting Development in a Changing World. Available online at: https://www.gfdrr.org/sites/default/files/Brochure%20for%20Urban%20Resilience%20flagship%20report.pdf

Google Scholar

Glaum, P., Simao, M.-C., Vaidya, C., Fitch, G., and Iulinao, B. (2017). Big city Bombus: using natural history and land-use history to find significant environmental drivers in bumble-bee declines in urban development. R. Soc. Open Sci. 4:170156. doi: 10.1098/rsos.170156

PubMed Abstract | CrossRef Full Text | Google Scholar

Goertzen, D., and Suhling, F. (2013). Promoting dragonfly diversity in cities: major determinants and implications for urban pond design. J. Insect Conserv. 17, 399–409. doi: 10.1007/s10841-012-9522-z

CrossRef Full Text | Google Scholar

Gustafsson, K. M., Agrawal, A. A., Lewenstein, B. V., and Wolf, S. A. (2015). The monarch butterfly through time and space: the social construction of an icon. Bioscience 65, 612–622. doi: 10.1093/biosci/biv045

CrossRef Full Text | Google Scholar

Hall, D. M., Camilo, G. R., Tonietto, R. K., Ollerton, J., Ahrn,é, K., Arduser, M., et al. (2017). The city as a refuge for insect pollinators. Conserv. Biol. 31, 24–29. doi: 10.1111/cobi.12840

PubMed Abstract | CrossRef Full Text | Google Scholar

Hallmann, C. A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., et al. (2017). More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12:0185809. doi: 10.1371/journal.pone.0185809

PubMed Abstract | CrossRef Full Text | Google Scholar

Hartig, T., and Kahn, P. H. Jr. (2016). Living in cities, naturally. Science 352, 938–940. doi: 10.1126/science.aaf3759

PubMed Abstract | CrossRef Full Text | Google Scholar

Hladik, M. L., and Kolpin, D. W. (2015). First national-scale reconnaissance of neonicotinoid insecticides in stream across the USA. Environ. Chem. 13, 12–20. doi: 10.1071/EN15061

CrossRef Full Text | Google Scholar

Hostetler, M., Allen, W., and Meurk, C. (2011). Conserving urban biodiversity? Creating green infrastructure is only the first step. Landscape Urban Planning 100, 369–371. doi: 10.1016/j.landurbplan.2011.01.011

CrossRef Full Text | Google Scholar

Intergovernmental Science-Policy Platform on Biodiversity Ecosystem Services (IPBES) (2019). Global Assessment Report on Biodiversity and Ecosystem Services. Available online at: https://www.ipbes.net/news/Media-Release-Global-Assessment

Google Scholar

Ives, C. D., Lentini, P. E., Threlfall, C. G., Ikin, K., Shanahan, D. F., Garrard, G. E., et al. (2016). Cities are hotspots for threatened species. Global Ecol. Biogeography 25, 117–126. doi: 10.1111/geb.12404

CrossRef Full Text | Google Scholar

Jarosz, L. (2008). The city in the country: growing alternative food networks in Metropolitan areas. J. Rural Stud. 24, 231–244. doi: 10.1016/j.jrurstud.2007.10.002

CrossRef Full Text | Google Scholar

Johnston, M. K., Hasle, E. M., Klinger, K. R., Lambruschi, M. P., Derby Lewis, A., Stotz, D. F., et al. (2019). Estimating milkweed abundance in metropolitan areas under existing and user-defined scenarios. Front. Ecol. Evol. Conserv. doi: 10.3389/fevo.2019.00210. [Epub ahead of print].

CrossRef Full Text | Google Scholar

LaPoint, S. D., Gallery, P., Wikelski, M., and Kays, R. (2015) Animal behavior, cost-based corridors, real corridors. Landscape Ecol. 28, 1615–1630. doi: 10.1007/s10980-013-9910-0

CrossRef Full Text | Google Scholar

Lister, B. C., and Garcia, A. (2018). Climate-driven declines in arthropod abundance restructure a rainforest food web. Proc. Natl. Acad. Sci. U.S.A. 115, E10397–E10406. doi: 10.1073/pnas.1722477115

PubMed Abstract | CrossRef Full Text | Google Scholar

Lovell, S. T. (2010). Multifunctional urban agriculture for sustainable land use planning in the United States. Sustainability 2, 2499–2522. doi: 10.3390/su2082499

CrossRef Full Text | Google Scholar

Luck, G. W. (2007). A review of the relationships between human population density and biodiversity. Biol. Rev. Cambridge Philos. Soc. 82, 607–645. doi: 10.1111/j.1469-185X.2007.00028.x

PubMed Abstract | CrossRef Full Text | Google Scholar

McMahan, L. (2006). Understanding cultural reasons for the increase in both restoration efforts and gardening with native plants. Native Plants J. 7, 31–34. doi: 10.1353/npj.2006.0013

CrossRef Full Text | Google Scholar

Miller, J. R., and Hobbs, R. J. (2002). Conservation where people live and work. Conserv. Biol. 16, 330–337. doi: 10.1046/j.1523-1739.2002.00420.x

CrossRef Full Text | Google Scholar

Morey, P. S., Gese, E. G., and Gehrt, S. (2007). Spatial and temporal variation in the diet of coyotes in the Chicago Metropolitan Area. Am. Midland Natural. 158, 147–161. doi: 10.1674/0003-0031(2007)158;[147:SATVIT]2.0.CO;2

CrossRef Full Text | Google Scholar

Nash, R. (1967). Wilderness and the American Mind. New Haven: Yale University Press.

Google Scholar

Pearson, A. R., Schuldt, J. P., Romero-Canyas, R., Ballew, M. T., and Larson-Konar, D. (2018). Diverse segments of the US public underestimate the environmental concerns of minority and low-income Americans. PNAS 115, 12429–12434. doi: 10.1073/pnas.1804698115

PubMed Abstract | CrossRef Full Text | Google Scholar

Pyle, R. (1978). The extinction of experience. Horticulture 56, 64–67. doi: 10.1002/j.2164-4918.1978.tb04671.x

CrossRef Full Text | Google Scholar

Pyle, R. (1993). The Thunder Tree: Lessons From an Urban Wildland. Boston: Houghton Mifflin.

Google Scholar

Rosenzweig, M. L. (2003). Reconciliation ecology and the future of species diversity. Oryx 37, 194–205. doi: 10.1017/S0030605303000371

CrossRef Full Text | Google Scholar

Schensul, J. J., and LeCompte, M. D. (2013). Designing and Conducting Ethnographic Research: An Introduction, Vol. 1. New York, NY: AltaMira Press.

Google Scholar

Schultz, C. B., Brown, L. M., Pelton, E., and Crone, E. E. (2017). Citizen science monitoring demonstrates dramatic declines of monarch butterflies in western North America. Biol. Conserv. 214, 343–346. doi: 10.1016/j.biocon.2017.08.019

CrossRef Full Text | Google Scholar

Seewagen, C. L., Sheppard, C. D., Slayton, E. J., and Guglielmo, C. G. (2011). Plasma metabolites and mass changes of migratory landbirds indicate adequate stopover refueling in a heavily urbanized landscape. Condor 113, 284–297. doi: 10.1525/cond.2011.100136

CrossRef Full Text | Google Scholar

Semmens, B. X., Semmens, D. J., Thogmartin, W. E., Wiederholt, R., López-Hoffman, L., Diffendorfer, J. E., et al. (2016). Quasi-extinction risk and population targets for the Eastern, migratory population of monarch butterflies (Danaus plexippus). Sci. Rep. 6:23265. doi: 10.1038/srep23265

PubMed Abstract | CrossRef Full Text | Google Scholar

Soga, M., and Gaston, K. J. (2016). Extinction of experience: the loss of human-nature interactions. Front. Ecol. Environ. 14, 94–101. doi: 10.1002/fee.1225

CrossRef Full Text | Google Scholar

Tam, K. C., and Bonebrake, T. C. (2016). Lepidoptera-habitat relationships in urban parks. Urban Ecosystems 19:721. doi: 10.1007/s11252-015-0484-2

CrossRef Full Text | Google Scholar

Taylor, D. E. (2016). The Rise of the American Conservation Movement: Power, Privilege, and Environmental Protection. Durham: Duke University Press Books. doi: 10.1215/9780822373971

CrossRef Full Text | Google Scholar

Thogmartin, W. E., López-Hoffman, L., Rohweder, J., Diffendorfer, J., Drum, R., Semmens, D., et al. (2017). Restoring monarch butterfly habitat in the Midwestern US: ‘all hands on deck'. Environ. Res. Lett. 12:074005. doi: 10.1088/1748-9326/aa7637

CrossRef Full Text | Google Scholar

Tommasi, D., Miro, A., Higo, H., and Winston, M. (2004). Bee diversity and abundance in an urban setting. Can. Entomol. 136, 851–869. doi: 10.4039/n04-010

CrossRef Full Text | Google Scholar

Tuan, Y.-F. (1978). The city: its distance from nature. Geograph. Rev. 68, 1–12. doi: 10.2307/213507

CrossRef Full Text | Google Scholar

Turner, W. R., Nakamura, T., and Dinetti, M. (2004). Global urbanization and the separation of humans from nature. Bioscience 54, 585–590. doi: 10.1641/0006-3568(2004)054[0585:GUATSO]2.0.CO;2

CrossRef Full Text | Google Scholar

U.S. Fish and Wildlife Service (2017). Survey Protocols for the Rusty Patched Bumble Bee. U.S. Fish and Wildlife Service, Version, 1.1. Available online at: https://www.fws.gov/midwest/endangered/insects/rpbb/pdf/SurveyProtocolsRPBB28Feb2018.pdf

Google Scholar

UN DESA (2018). World Urbanization Prospects: 2018. Available online at: https://population.un.org/wup/Publications/Files/WUP2018-KeyFacts.pdf

Google Scholar

Van Horn, G., and Aftandilian, D. (2015). City Creatures: Animal Encounters in the Chicago Wilderness. Chicago: University of Chicago Press.

Google Scholar

West, P., Igoe, J., and Brockington, D. (2006). Parks and peoples: the social impact of protected areas. Ann. Rev. Anthropol. 35, 251–77. doi: 10.1146/annurev.anthro.35.081705.123308

CrossRef Full Text | Google Scholar

Wickman, J., Homer, C., Vogelmann, J., McKerrow, A., Mueller, R., Herold, N., and Coulston, J. (2014). The multi-resolution land characteristics (MRLC) consortium-−20 years of development and integration of USA national land cover data. Remote Sens. 6, 7424–7441. doi: 10.3390/rs6087424

CrossRef Full Text | Google Scholar

Williams, R. (1975). The Country and the City. Oxford: Oxford University Press.

PubMed Abstract | Google Scholar

Wirth, L. (1938). Urbanism as a way of life. Am. J. Sociol. 44, 1–24. doi: 10.1086/217913

CrossRef Full Text | Google Scholar

Wolch, J. R., Byrne, J., and Newell, J. P. (2014). Urban green space, public health, and environmental justice: the challenge of making cities ‘just green enough'. Landscape Urban Planning 125, 234–244. doi: 10.1016/j.landurbplan.2014.01.017

CrossRef Full Text | Google Scholar

World Wildlife Fund (2018). Living Planet Report: Aiming Higher. eds M. Grooten and R. E. A. Almond. Gland: WWF.

Google Scholar

Zhang, W., Goodale, E., and Chen, J. (2014). How contact with nature affects children's biophilia, 420 biophobia and conservation attitude in China. Biol. Conserv. 177, 109–116. doi: 10.1016/j.biocon.2014.06.011

CrossRef Full Text | Google Scholar

Keywords: urban, ecology, wildlife, conservation, culture, monarch, pollinators

Citation: Derby Lewis A, Bouman MJ, Winter AM, Hasle EA, Stotz DF, Johnston MK, Klinger KR, Rosenthal A and Czarnecki CA (2019) Does Nature Need Cities? Pollinators Reveal a Role for Cities in Wildlife Conservation. Front. Ecol. Evol. 7:220. doi: 10.3389/fevo.2019.00220

Received: 29 December 2018; Accepted: 24 May 2019;
Published: 21 June 2019.

Edited by:

Jay E. Diffendorfer, United States Geological Survey, United States

Reviewed by:

Scott Black, Xerces Society for Invertebrate Conservation, United States
Mohammad Imam Hasan Reza, Presidency International School, Bangladesh

Copyright © 2019 Derby Lewis, Bouman, Winter, Hasle, Stotz, Johnston, Klinger, Rosenthal and Czarnecki. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Abigail Derby Lewis, aderby@fieldmuseum.org