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Urban forest biodiversity and cardiovascular disease: Potential health benefits from California’s street trees

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the fifth most popular, decreases evenness and exposure to biodiversity because the change in the Shannon Index is -0.39 or -0.30. The effect is similar for both scenarios, suggesting there are not large biodiversity benefits to uniform plantings of slightly less popular genus. In con- trast, if plantings are spread evenly across just two genera, this increases exposure to biodiver- sity and brings potential avoided mortality benefits of $89 per zip code for heart disease and $32 per zip code for stroke. Further increasing the diversity of plantings to ten trees each of five genera results in very large benefits of $1,183 per zip code for heart disease and $425 per zip code for stroke. Net benefits from tree planting in Los Angeles We add benefits from avoided mortality to benefits from eco-services from trees in Los Ange- les, with the low estimate at $38 per tree per year to the high estimate of $56 per tree per year in the city of Los Angeles [59,60]. We can compare total annual benefits to total annual costs to calculate net benefits. Annualized lifetime planting and maintenance costs were estimated at $52–79 per tree per year [73,74], assuming a discount rate of 7%, allowing for extra costs associated with concrete tree wells, poor soil, and supplemental watering, and using an esti- mated Los Angeles street tree lifetime of 30 years based on allometric equations for eight spe- cies in our dataset. We begin by assuming there are no additional costs from increasing the diversity of street tree plantings by up to ten genera, though this may be unlikely if local nurs-

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eries fail to stock a sufficiently diverse set of seedlings. Given these assumptions, the total direct cost for planting fifty trees is $2,599–3,950 per zip code. When considering total benefits, from avoided mortality and ecosystem services, increasing diversity increases the return on a tree-planting investment. For the lower planting cost esti- mate, net benefits (benefits–cost) are positive when planting is evenly split across two or more genera. For the higher cost estimate, net benefits are positive when planting is evenly split across five or more genera. Note that these benefits do not include those associated with self- reported positive emotions and restoration in physical and mental health [75,76], encouraged physical activity [77,78], lower obesity reports and improved social cohesion [6], and reduced asthma in young children [79] with exposure to greenspace or benefits to other species, such as birds [80]. Cost-effectiveness of increasing biodiversity to combat cardiovascular disease Next, we consider the cost-effectiveness of this intervention within the context of preventing cardiovascular disease. Cost-effectiveness compares the incremental change in the cost of a policy, as compared to the standard approach, and the incremental change in benefits. Given large uncertainties, assessing the cost-effectiveness of a policy to prevent cardiovascular disease is difficult to assess in the best of circumstances [81]. In our context, we are working outside of an experimental framework, so our estimates should be interpreted with caution.

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We begin by assuming a tree-planting initiative without a biodiversity mandate is the stan- dard approach. We simplify this to be planting the top genus, only. The incremental change in policy is increasing the biodiversity of plantings. The cost of increasing the diversity of plant- ings is unknown. A very rough estimate could be to include a 10–50% surcharge on the cost of a seedling to reflect administrative and transport costs to locate a vendor selling seedlings locally unavailable and transporting the seedlings to Los Angeles. This changes the planting cost range to $53–88 per tree or $2626–4380 per zip code, giving an incremental change of $27–417 per zip code. The gain would be the difference in benefits from planting only the top genus and the alternative scenario. This works out to $1,129–3,782 in total benefits from PLOS ONE Biodiversity and cardiovascular disease PLOS ONE | https://doi.org/10.1371/journal.pone.0254973 November 3, 2021 16 / 23

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mortality from cardiovascular disease, where the lower number reflects the Top 2 scenario and the higher number the Top 10 scenario. In terms of cost-effectiveness, this is a return of $2.70- $140.07 for each dollar invested. The lower estimate is similar to results from a simulation that estimated medical cost savings in return for investing in parks and trails [82] and a compre- hensive workplace wellness program [83]. This simulation suggests that if our effect sizes are replicated within a causal framework, increasing the diversity of tree planting may be a cost- effective way to prevent cardiovascular disease. Conclusion Cardiovascular disease is the most common cause of mortality in the United States. Though management of blood pressure has improved over the last two decades, risk factors like obesity and diabetes remain challenging to address. Many population-based epidemiological studies have found an association between exposure to greenspace and lower cardiovascular risk. Numerous experimental studies of Shinrin-yoku and similar means of sustained forest expo- sure point to acute physiological changes after walking in a forest. Beyond the extent or quan- tity of general greenspace exposure, the quality of biodiversity may influence health outcomes via enhanced immune functioning and thus reduce mortality risks of diseases connected to proper immune functioning. Our paper examines whether greater biodiversity within urban forests in California is asso- ciated with lower cerebrovascular and cardiovascular mortality. Using mortality data from

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2010–2018, we find that increasing the diversity of an urban forest by one standard deviation (0.64) is associated with a decrease in the mortality rate of 21.4 per hundred thousand for heart disease or 13% and 7.7 per hundred thousand for stroke or 16%. The relationship is linear, though having very diverse forests may offer additional protection. We explore possible mech- anisms and fail to find support that our effects are driven by psychological restoration or dilu- tion of disease risk. We conclude that enhanced immune functioning seems the most likely pathway. As stated earlier, the role of actual biodiversity within green spaces and urban forests on human health outcomes remain highly unexplored. Our paper is the first to assess how bio- diversity exposure is associated with cardiovascular health. Future research should use a causal framework to test the relationship between biodiversity and human health and potential mechanisms. The strong association between urban forest diversity and reduced cardiovascular disease mortality suggests that tree-planting may be a useful policy lever to address cardiovascular dis- ease. Benefits from planting street trees typically do not include avoided mortality from heart disease and stroke. A policy simulation of different planting scenarios for the city of Los Ange- les found that even small efforts to increase planting diversity, such as splitting new plantings evenly across more than two genera, may be a cost-effective policy tool to reduce the risk of

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cerebrovascular and cardiovascular disease. Though our estimates include many uncertainties, we find that increasing the biodiversity of existing tree planting initiatives may beget a return of $2.70-$140.07 for each dollar invested. The lower estimate is similar in magnitude to the return on investment parks and trails and a comprehensive workplace wellness program. Future research should use more comprehensive data on urban forest biodiversity, such as the future TreeKeeper data from LA, and an experimental design that allows for causal infer- ence to directly test the relationship between biodiversity and prevention of cardiovascular dis- ease and mortality. Work is also needed to better understand the dose-response function for chronic exposure to biodiversity when living near greenspace. Moving forward in this way could enrich our conception of “green prescriptions,” improve policy targeting to communi- ties with inequitable access to biodiversity, and encourage cost-effective policy investments. PLOS ONE Biodiversity and cardiovascular disease PLOS ONE | https://doi.org/10.1371/journal.pone.0254973 November 3, 2021 17 / 23

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Supporting information S1 Fig. Urban forest diversity and tree per hundred thousand people. Data for 857 Califor- nia zip codes in Heart Disease sample from consortium of private tree maintenance compa- nies. (TIF) S2 Fig. Urban forest diversity, socioeconomic characteristics, and pollution burden. Data for 551 California zip codes in Heart Disease sample matched with income data from the American Community Survey and pollution burden data from the CalEnviroScreen 3.0. Shannon Index calculated from tree data from consortium of private tree maintenance compa- nies. (TIF) S3 Fig. Urban forest diversity and confirmed Lyme disease by CA county. Data for 22 Cali- fornia counties with forest biodiversity data. Lyme disease incidence calculated for period 2009–2018 by California Department of Public Health. Shannon Index calculated from tree data from consortium of private tree maintenance companies. (TIF) S1 Table. Summary statistics for sociodemographics and pollution burden. Data for 551 California zip codes in Heart Disease sample matched with socioeconomic data from 2010 Census, 2012–2016 American Community Survey, 2000 Decennial Census, and Longitudinal Employer-Household Dynamics (LEHD), and CalEnviroScreen 3.0. (DOCX) S2 Table. Spatial auto-regression model for each year. Estimates from a linear regression with spatially correlated error terms estimated using the spregress command (McMillan et al. 2008). Each column corresponds to a year of data. Coefficients reported are for the total

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effect of the Shannon index on mortality. Panel A is Heart Disease mortality and panel B is Stroke mortality. Estimates from 2018 also reported in main text. ��� p<0.001, �� p<0.01, � p<0.05. (DOCX) S3 Table. Subsample analysis by two-digit zip-code. Estimates from linear regression where the outcome variable is mortality rate per zip code-year, measured in deaths per 100,000 indi- viduals. Column one repeats the main estimate. Columns two through seven are spatial sub- samples for each two-digit zip code area, from 90 to 95. Regressions include year and 3-digit zip-code fixed effects, standard errors are clustered by 3-digit zip-code and reported in paren- theses ��� p<0.001, �� p<0.01, � p<0.05. (DOCX) S1 File. (CSV) S2 File. (CSV) S3 File. (CSV) S1 Data. (DOCX) PLOS ONE Biodiversity and cardiovascular disease PLOS ONE | https://doi.org/10.1371/journal.pone.0254973 November 3, 2021 18 / 23

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Acknowledgments We would like to thank Cindy Blain (Executive Director of California ReLeaf), Nancy J. Hughes (Executive Director of California Urban Forests Council), and Rachel Malarich (City Forest Officer of City of Los Angeles) for helpful discussions regarding the costs and challenges of planting urban trees in California. We would also like to thank Michael Huggins and Viet Nguyen for help with the urban for- est characteristics data. Finally, we would like to thank the private tree companies who shared their data with us and made this analysis possible. Author Contributions Conceptualization: John J. Giacinto, Jacqueline Doremus. Data curation: John J. Giacinto, G. Andrew Fricker. Formal analysis: John J. Giacinto, Jacqueline Doremus. Funding acquisition: Matthew Ritter, Jenn Yost. Investigation: John J. Giacinto, Jacqueline Doremus. Methodology: John J. Giacinto, Jacqueline Doremus. Project administration: Jenn Yost, Jacqueline Doremus. Resources: G. Andrew Fricker, Matthew Ritter, Jenn Yost. Software: G. Andrew Fricker. Supervision: Matthew Ritter, Jenn Yost, Jacqueline Doremus. Validation: John J. Giacinto, Jacqueline Doremus. Visualization: John J. Giacinto, G. Andrew Fricker, Jacqueline Doremus. Writing – original draft: John J. Giacinto, Jacqueline Doremus. Writing – review & editing: John J. Giacinto, Jacqueline Doremus. References 1. Center for Disease Control (CDC). Vital Signs: Avoidable Deaths From Heart Disease, Stroke, and Hypertensive Disease–United States 2001–2010. 2013 https://www.cdc.gov/mmwr/preview/ mmwrhtml/mm6235a4.htm?s_cid=mm6235a4_w.

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