HUMAN HEALTH AND ENVIRONMENTAL SUSTAINABILITY IN PATHOGENIC LANDSCAPES: FEEDBACKS AND SOLUTIONS A DISSERTATION SUBMITTED TO THE DEPARTMENT OF BIOLOGY AND THE COMMITTEE ON GRADUATE STUDIES OF STANFORD UNIVERSITY IN PARTIAL FUFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY ISABEL JEAN JONES AUGUST 2020 © 2020 by Isabel Jean Jones. All Rights Reserved. Re-distributed by Stanford University under license with the author. This work is licensed under a Creative Commons Attribution- Noncommercial 3.0 United States License. http://creativecommons.org/licenses/by-nc/3.0/us/ This dissertation is online at: http://purl.stanford.edu/fv856hm0269 ii I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Giulio De Leo, Primary Adviser I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Erin Mordecai I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Stephen Palumbi Approved for the Stanford University Committee on Graduate Studies. Stacey F. Bent, Vice Provost for Graduate Education This signature page was generated electronically upon submission of this dissertation in electronic format. An original signed hard copy of the signature page is on file in University Archives. iii Abstract Feedbacks between human health, well-being, and environmental sustainability are increasingly well recognized, but evidence on ActionAble solutions to leverAge tHese feedbAcks And improve their outcomes is limited. And yet, the recently adopted United NAtions SustainAble Development GoAls compel decision makers to achieve health for all people while reducing poverty and conserving nature. This dissertation attempts to fill this urgent research gap and empirically assess feedbacks between human health and the environment from two perspectives: (i) environmentAl drivers of diseAse in cHAnging lAndscApes, And (ii) consequences of Human HeAltH and well-being on environmental change and conservation outcomes. But first, using synthesis science, we describe the environmental components of the world’s most burdensome human parasitic and infectious diseases, then assess a specific type of ecosystem service – natural enemies of human infections – as a sustainable tool to reduce some communicable diseases. Then, we Assess feedbAcks between HumAn HeAltH And environmental sustainability through two datA-ricH cAse studies. First, in the SenegAl River BAsin, a region hyperendemic for scHistosomiasis diseAse, we assess ecologicAl associations and spAtial scAles of humAn diseAse risk. In this region, scHistosomiasis diseAse, which is transmitted to humans by freshwater snail hosts, can be caused by two species of schistosome parasites (and their two unique snail hosts). The World HeAltH OrgAnizAtion currently recommends tHAt snAil control be implemented in endemic areas to curb transmission. However, snail control methods rarely take into consideration the unique transmission dynAmics of co-endemic species, which could interfere with control outcomes for one or both species. So here we ask a critical question: whAt is tHe spatial scale and ecological correlates of schistosomiasis risk, considering two distinct schistosome species in a co- endemic landscape? We find specific, yet divergent, ecologicAl correlAtes And spAtiAl scAles of risk for eAcH species. UltimAtely, these findings can be used to design ecological levers for health (like snAil control) thAt best reflect the unique transmission ecology the targeted species. Second, in rural Borneo, we assess the impAct of a 10-year, on-the-ground intervention aiming to improve Human health care access in order to curb illegal logging in protected forests, and ask: Is healthcare an effective lever for conservation? Using earth observation, household surveys, and clinic data records, we find that the intervention provided health care access for more thAn 28,000 patients and averted >27km2 forest loss (~70% reduction compAred to controls), thus improving human health and well-being, and simultaneously preserving globally important forest carbon. In conclusion, this dissertation shows thAt, by recognizing and embracing complex mecHAnisms driving healtH-environment feedbacks, we can identify effective ecological levers for human health, and health levers for conservation. iv Acknowledgements Many people Helped tHis dissertAtion come together, but there are two people thAt facilitated and supported each and every part: Giulio De Leo and Susanne Sokolow. To my generous advisor and powerhouse mentor, many tHAnks for your continued personAl And AcAdemic support, and for always putting my well-being ahead of my work. I also hAd an excellent dissertation committee thAt cHAllenged and supported me, so thAnk you to Erin MordecAi and Steve PAlumbi. Andy, many thAnks to Steve Luby and Rodolfo Dirzo for joining my oral defense committee. Outside of Stanford, no smAll amount of guidAnce, patient teaching, and friendship came from Chelsea Wood, SkylAr Hopkins, And Andy MAcDonAld. ThAnks Also to tHe NCEAS SNAPP working group, “Ecological Levers for Health”, for welcoming me into an incredible community of reseArcHers thAt I was first intimidAted by but can now call friends and colleagues. The most rewArding aspect of my reseArcH experience wAs the opportunity to work with reseArcHers, conservation practitioners, health care providers, activists, and community members working on- the-ground, around-the-clock to make real positive change to the daily lives of people, to protect and restore the natural world, and to enact climate change mitigation. To that end, thank you to the UpstreAm Alliance teAm in Senegal for supported me during five amAzing field trips to the Senegal River Basin, to HeAltH In Harmony in PortlAnd and Alam Sehat Lestari in Borneo for endless inspiration, to MArtinA LAidemitt and Dr. SAm Loker for welcoming to join in and leArn from their incredible long-term field reseArcH at Lake Victoria in Kenya, and to PIVOT in MadAgAscAr for generously Hosting me for a truly unique reseArcH experience in IfanAdianA. AndreA Lund was tHe best dissertAtion partner and friend to have along the way – thAnk you for reminding me thAt “a good dissertation is a done dissertation”. My friends – the bAsketbAll champions in the De Leo Lab, Tim White, SerenA Lomonico, A2 Andy ChAmberlAin & Alex Smith, and Shirel Kahane-Rapport – made life in Monterey fun And interesting, And convinced me to stay put in this mAgical place as long as possible, wHicH is exActly wHAt I’ll do. Luke NetscH has been a stellar partner and has made Monterey and its beaches and mountains a lovely home for us. My fAmily – Laurel, Robert, AmAndA, HannAH, Chris, Kyle, JeAn, Emer, DiAne – remind me every day what’s most important. RutH, you Are tHe best. v vi Table of Contents Abstract ............................................................................................................................. iv Acknowledgements .................................................................................................................... v Introduction ....................................................................................................................... 1 Chapter 1 : Biodiversity and environmentAl persistence of the world’s most burdensome infectious and parasitic diseAses ........................................................................................ 10 Chapter 2 : Enemy of my enemy: NAtural enemies for sustAinable control of humAn infections ........................................................................................................................... 28 Chapter 3 : Divergent ecologicAl drivers and spatiAl scAles of risk for S. haemAtobium And S. mAnsoni in a co-endemic lAndscApe ....................................................................... 63 Chapter 4 : Improving rural heAlth cAre reduces illegal logging and conserves cArbon in A tropicAl forest .................................................................................................................. 98 Conclusion ...................................................................................................................... 156 vii List of Illustrations Figure 1.1. AssociAtions between duration of infectious stAges in the environment, transmission strategies, control strategies, host ranges, and global cAses of diseAse ....... 23 Figure 2.1. NAtural enemies of humAn infectious diseAses in the environment .............. 57 Figure 2.2. Reports of mosquito vector resistAnce to insecticides over time (A) and natural enemies of mosquitoes (B) .................................................................................. 58 Figure 3.1. Study locAtion (A); examples of overheAd drone imAgery and high-resolution imAge clAssificAtion into dominant aquatic habitAt types (B–C) ..................................... 88 Figure 3.2. EstimAted mArginal meAns for Bulinus spp. (A–B) and Biomphalaria pfeifferi (C–D) snails in three dominant aquatic HAbitAt types ...................................................... 89 Figure 3.3. VisualizAtion of experimentAl design to explore scAle of diseAse transmission risk (A); correlAtion between non-emergent vegetAtion and S. haematobium And S. mansoni infection