Human Health Impacts of Ecosystem Alteration

PERSPECTIVE PERSPECTIVE Human health impacts of ecosystem alteration

Samuel S. Myersa,b,1,LynneGafﬁkinc, Christopher D. Golden b, Richard S. Ostfeld d,KentH.Redforde,2, Taylor H. Rickettsf, Will R. Turnerg, and Steven A. Osofskyh aDepartment of Environmental Health, Harvard School of Public Health, and bHarvard Center for the Environment, Harvard University, Cambridge, MA 02138; cEvaluation and Research Technologies for Health Inc., Woodside, CA 94062; dCary Institute of Ecosystem Studies, Millbrook, NY 12545; eWildlife Conservation Society Institute and hWildlife Health and Health Policy Program, Wildlife Conservation Society, Bronx, NY 10460; fGund Institute for Ecological Economics, University of Vermont, Burlington, VT 05405; and gBetty and Gordon Moore Center for Science and Oceans, Conservation International, Arlington, VA 22202

Edited by William C. Clark, Harvard University, Cambridge, MA, and approved October 11, 2013 (received for review October 31, 2012)

Human activity is rapidly transforming most of Earth’s natural systems. How this transformation is impacting human health, whose health is at greatest risk, and the magnitude of the associated disease burden are relatively new subjects within the ﬁeld of environmental health. We discuss what is known about the human health implications of changes in the structure and function of natural systems and propose that these changes are affecting human health in a variety of important ways. We identify several gaps and limitations in the research that has been done to date and propose a more systematic and comprehensive approach to applied research in this ﬁeld. Such efforts could lead to a more robust understanding of the human health impacts of accelerating environmental change and inform decision making in the land-use planning, environmental conservation, and public health policy realms.

global change | ecosystem services | ecology | planetary boundaries | ecological footprint

At least since Hippocrates wrote On Airs, has given rise to the definition of a new geo- has coincided with large improvements in Waters, and Places, the natural environment logical epoch: the Anthropocene (2). most health indices globally. has been viewed as an important determi- The arrival of the Anthropocene presents Here we explore our current understand- nant of human health. However, over the last an uncertain future, not only for the biosphere, ing of the human health impacts of alter- century, the field of environmental health but for humanity itself. There is widespread ations in the structure and functioning of has focused increasingly on quantifying ex- debate about the ability of an altered global Earth’s natural systems. Our goals are to (i) posure–response relationships for toxins en- environment to meet the needs of a growing illustrate what is currently known, (ii)identify countered in the human-dominated environ- and prospering human population. Health is gaps and limitations that can be addressed by ment: from an initial focus on workplace one dimension of human well-being that has future research efforts, (iii)addressthescaleof exposures, to a population-level focus on ra- received particular attentioninthisdiscussion. the health burden associated with changes to diation, heavy metals, air and water pollution, In 2005, for example, 1,360 experts from 95 natural systems, and (iv) propose a research and more recently, to exposure to endocrine- countries produced The Millennium Ecosys- approach that strengthens the practice of both tem Assessment (MA), a consensus document public health and environmental conservation. disrupting chemicals. Over this period, rela- ’ tively little attention has been paid to how evaluating the state of the planet s ecosystems. The authors concluded that “any progress Highlights of the Recent Literature changes in the structure and function of achieved in addressing the Millennium Devel- Other reviews have laid out a more complete Earth’s natural systems might affect human opment Goals of poverty and hunger eradica- summary of the existing literature than health. Growing evidence that changes in tion,improvedhealth,andenvironmental we intend here (5). As these reviewers have these natural systems can affect human health sustainability is unlikely to be sustained if most noted, the literature exploring connections in a variety of important ways and the increas- of the ecosystem services on which humanity between human health and ecological altering pace and extent of these changes has relies continue to be degraded” (3). At the ation includes multiple studies scattered prompted this Perspective. In it, we review same time, the Director-General of the World fi across a variety of disciplines that leave many current understanding of this eld, identify Health Organization underscored that of the most important relationships incom- some of its gaps and limitations, and suggest “Nature’s goods and services are the ultimate pletely characterized. Despite its patchy na- an approach to expanding our understanding. foundations of life and health” (4). ture, in aggregate, this work is convincing that Human activity is transforming nearly all Despite the intuitive importance of natural of Earth’s natural systems. With the human systems to human health, the empirical evi- Author contributions: S.S.M., K.H.R., and S.A.O. designed research; population now exceeding 7 billion people and dence to support these claims has been rel- S.S.M., L.G., C.D.G., and S.A.O. performed research; and S.S.M., L.G., rapid growth in per capita consumption of atively thin. On one hand, natural systems C.D.G., R.S.O., K.H.R., T.H.R., W.R.T., and S.A.O. wrote the paper. ’ goods and services, humanity sgrowing provide a suite of “ecosystem services” includ- The authors declare no conflict of interest. ’ ecological footprint is altering the planet s ing nutrition, purification of water, protection This article is a PNAS Direct Submission. land cover, rivers and oceans, climate sys- from natural hazards, and reduction of some 1To whom correspondence should be addressed. E-mail: smyers@ tem, biogeochemical cycles, and the function- infectious diseases (3). On the other hand, ex- hsph.harvard.edu. ing of its ecosystems (1). This suite of changes tensive human alteration of the natural world 2Present address: Archipelago Consulting, Portland, ME 04112.

www.pnas.org/cgi/doi/10.1073/pnas.1218656110 PNAS | November 19, 2013 | vol. 110 | no. 47 | 18753–18760 Downloaded by guest on October 1, 2021 there are significant linkages between the consumption of wild meat (35) can provide hosts that amplify transmission (competent structure and function of natural systems and public health benefits as they provide new land hosts), resulting in decreased exposure to a variety of human health outcomes. Here, we for agriculture and, in the case of bushmeat, vector-borne disease (59, 60). Recent modeling provide an overview of the types of relation- rich sources of nutrients, but these activities work suggests the dilution effect may account ships that have been well studied and estab- also create the potential for zoonotic infections for reduced malaria transmission in diverse lished as a prelude to exploring the gaps, to move from animal to human populations. regions of the Brazilian Amazon as well (61). limitations, and areas requiring further study. There is compelling evidence that these mech- For such an effect to be generalizable across With roughly half the temperate and anisms played the central role in initial out- different diseases and ecosystems, it must tropical forests cut down, nearly half the ice- breaks of HIV and Ebola virus, as well as often be the case that hosts that are more free, desert-free terrestrial landscape con- several lesser-known zoonoses (36). The effective at transmitting pathogens (compe- verted to croplands or pasture, and more than power of these shifts in animal–human inter- tent hosts) tend to persist and less competent 800,000 dams impeding the flow through actions to affect disease transmission helps to ones disappear as diversity declines. Some more than 60% of the world’s rivers, alter- explain the fact that roughly 75% of emerging recent research suggests that immunological ations to our planet’s land use and land cover infectious diseases are zoonoses (37). tolerance, and hence high host competence, represent some of the most pervasive changes Some types of land-use change involve the tends to characterize the species that are in- humanity has made to Earth’s natural systems destruction of entire ecological systems and trinsically more likely to persist when di- (1). Some of these changes have clearly been the services that they provide. One example versity declines (62). Related research has associated with public health benefits. Early is the loss of coastal barrier systems in- indicated that hosts with a high intrinsic rate efforts to reduce malaria in the Tennessee cluding coastal mangroves, coral reefs, veg- of increase are both more ecologically re- Valley (6) and countries in sub-Saharan Africa etated dunes, and coastal wetlands. These silient and reservoir competent (58). Other including Nigeria (7) by draining swamps that systems can lessen storm surge and attenu- work has emphasized the idiosyncratic nature were habitat for mosquito vectors, for exam- ate wave energy, thereby reducing morbidity of particular disease/ecology relationships ple, proved very successful. The primary mo- and mortality from coastal storms or tsu- (63), and still other efforts have concluded that tivation for deforestation, dams, and irrigation namis (38–41). Their global destruction puts generalizations about the effect of biodiversity projects in many parts of the world has been to in harm’s way roughly a third of humanity on disease transmission have been premature increase the supply of food and clean energy— who live within 100 km of the shore and at (64). Clarifying the impacts of disruption of critical building blocks for public health. less than 50 m above sea level (42) at the natural systems on transmission of vector- However, some of the negative impacts of same time that sea level rise and more ex- borne disease and the extent to which such land-use change have become clear more treme tropical storms increase the threat of relationships can be generalized across dis- recently. Dams and irrigation projects cause storm surge and coastal flooding. Forest eases and ecosystems remains an important very large increases in the prevalence of cover may reduce flooding and land slide area for future research. schistosomiasis (8–10) and malaria (11, 12) activity during extreme storms (43). Wet- Reductions in biodiversity or the pop- in parts of Africa and South Asia. They also lands and forest watersheds can filter pol- ulation sizes of species can have other im- increase exposure to other vector-borne lutants and pathogens from surface water portant human health impacts unrelated to diseases associated with significant mor- supplies (44, 45); and, to some extent, forests infectious disease. Losses of potential sources bidity and mortality including Rift Valley filter particulates from the air (46–48). Most of pharmaceuticals, experimental models for fever, filariasis, leishmaniasis, dracunculosis, such health-related ecosystem services re- studying disease, and wild relatives of im- onchocerciasis, and Japanese encephalitis (13– main poorly characterized. portant food crops can all have far-reaching 16). Deforestation increases exposure to One of the most dynamic areas of research health consequences (65). Crop pollination malaria in Africa (17–21) and South America into health impacts of ecosystem changes is (by insects, birds, and bats inhabiting natural (20–26) but has less predictable impacts in Asia disease ecology. Disease ecology explores ecosystems) is critical in the production of (27–31)wheretherearemanymoreAnopheles comprehensively how changes in a whole asignificant fraction of both nutrients and vectors with less generalizable responses to suite of factors such as population dynamics, calories in the human diet (66, 67). A rela- reduced forest cover. In parts of Africa, forest movement, physiological state, species rich- tively new area of research indicates that cutting also alters the composition and density ness, and relative abundance of species within aquatic and terrestrial wildlife populations are of aquatic snail species in a manner that favors an ecological community can alter risks of an important dietary source of both micro- transmission of schistosomiasis (32). exposure to infectious diseases (49, 50). Re- and macronutrients. For example, if house- Some land-use changes affect disease ex- cently, disease ecologists have shown that the holds in a population in Madagascar were posure less directly. In Belize, for example, risk of West Nile virus exposure in the United unable to harvest wild meat for consumption, nutrient enrichment with nitrogen and phos- States rises as avian biodiversity falls (51, 52), their children would experience a 30% higher phorus from agricultural runoff hundreds of and, similarly, Lyme disease exposure in- risk of iron deficiency anemia—a condition miles upstream causes a change in the vege- creases with falling mammalian diversity (53– that increases the risk for sickness and death tation pattern of lowland wetlands that 55). In field experiments, exposure to hanta- from infectious disease, reduces IQ and favorsthemoreefficient malaria vector virus increases when mammalian diversity learning, and reduces lifelong capacity for Anopheles vestipennis over the less efficient falls (56). For Chagas disease in Panama and physical activity (68). There is growing vector Anopheles albimanus,leadingtoin- the Brazilian Amazon, risk of human expo- awareness that dwindling populations of creased malaria exposure among coastal sure is positively correlated with reduced marine and terrestrial wildlife may represent populations (33). mammalian species diversity (57, 58). This a nutritional crisis for many people who Land-use changes that alter human–wild- suite of findings has led to the proposal of cannot readily replace these foods with do- life interactions can be an important source a general principle of disease ecology—the mesticated species or fortified foods. of zoonotic disease. Human encroachment “dilution effect”—whereby a greater diversity Reduced access to fuel and water will also into wildlife habitat (34) and the hunting and of intermediate hosts can dilute the pool of have health impacts, although they may be

18754 | www.pnas.org/cgi/doi/10.1073/pnas.1218656110 Myers et al. Downloaded by guest on October 1, 2021 mediated through less direct causal chains. predicted sharp rises in the number of people particularly important in relation to climate PERSPECTIVE Forest clearing in many parts of the world displaced by combinations of these factors change, where multiple threats may increase has led to reduced access to fuel for cooking (84, 85). All of these outcomes represent sig- concurrently and the capacity for local ad- fires, creating a disproportionate burden on nificant public health threats, with impacts aptation may be the most important de- women and girls who are often responsible thatarelikelytobeexacerbatedbytheirin- terminant of the ultimate health impacts. for gathering such fuel wood. Water scarcity teractions in some regions. Finally, and perhaps most important, the can have direct impacts on health through literature on ecological change and human reduced water quality and access to sanita- Limitations health needs to be more specific about whose tion,aswellasbycreatinganadditionalwork We highlight four important limitations in the health is in question. A particular ecosystem burden on those who have to exert more literature to date. First, much of the existing alteration may provide health benefits for energy carrying or pumping water from its research on the human health impacts of one segment of a population while incurring source. The direct impacts of these types alterations in natural systems focuses narrowly health costs for another. A dam project, for — of scarcity on the health of individuals and on a single health outcome aparticularin- example, may provide a source of clean en- — families require better characterization. fectious disease, for example rather than fo- ergy or increased agricultural productivity The social and psychological impacts of cusing on the impacts of changes to a natural for some while increasing the risk of malaria ecological degradation are also described in system across severaldimensionsofhuman and schistosomiasis for others. Perhaps eco- the literature. A loss of a “sense of place” or health. The degradation of a particular economic development in general is improving identity, depression, and emotional stress have system can result in multiple simultaneous health for most of the world’s people while all been documented in people experiencing impacts on health (e.g., deforestation leading the poorest populations disproportionately degradation of the natural environment to increased malaria exposure and loss of ac- experience the negative impacts of degraded around them (69). On the positive side, ex- cess to wild foods). Equally important, eco- natural systems—a dynamic that would be perience in nature, as well as outdoor ex- system degradation can lead to significant invisible if looking only at aggregated data. A ercise, have been associated with increased health improvements for local communities. corollary to this point is that future gen- mental and physical well-being, as well as Indeed, improved health is often the motiva- erations may also bear a larger share of the enhanced cognitive functioning (70). Re- tion for converting natural ecosystems (e.g., burden of degraded natural systems. In the duced postoperative recovery times and expanding agriculture or building dams to case of climate change, for example, fossil lower analgesic requirements in hospital- improve access to food and water). Assessing fuel consumption may be associated with ized patients with access to a natural view the net health effects of such changes would large public health benefits as individuals through their room window point to a have more utility for conservation and public become less dependent on biomass burning deeply seeded relationship between the health policy and practice than the study of as a source of heat and cooking fuel, whereas natural world and the psycho-physiological only one dimension of health at a time. the large health costs associated with climatic dimensions of human health (71). A related challenge is the need to evaluate disruption will accrue primarily to future There is a growing literature exploring the the health consequences of the complex in- generations. human health impacts of altering another terplay of multiple contemporaneous envi- One way to think about this disparity in natural system—our planet’satmosphere ronmental changes. In many parts of the the way populations experience health im- and its climate. Human health impacts world, land-use change, resource scarcities, pacts from alterations in natural systems is to of anthropogenic climatic disruption include and climate change effects are likely to in- consider a refinement of Smith and Ezzati’s changes in exposure to heat stress, air pollu- teract to alter exposure to infectious diseases, “environmental risk transition” (86). Smith tion, respiratory allergens, infectious disease, access to food and water, protection from and Ezzati make a compelling case that, in and natural hazards, as well as increased water natural hazards, and even population dis- aggregate, household level environmental scarcity, food insecurity, and population displacement with its additional associated health risks (e.g., poor sanitation, indoor particulate placement. Geographic distributions of some impacts. Although these interactions can be exposures, and unsafe drinking water) are infectious diseases (particularly vector-borne represented schematically (Fig. 1), investi- reduced concurrent with economic devel- diseases like malaria) are shifting in response gating how they will interact in particular pla- opment. However, their characterization to changes in temperature and precipitation ces among particular people may require masks the winners and losers in this pro- (72–74). Outbreaks of water-borne and food- different research methodologies than those cess. Over the course of economic de- borne disease are linked to extreme pre- which have been applied to date. velopment, people replace complex, natural cipitation and heat events (75–77). Allergenic A third limitation is that we have in- systems with engineered infrastructure and plants grown at elevated carbon dioxide pro- adequately explored how human adaptations markets as the source of food, water purifi- duce more pollen over a longer pollen season to ecosystem change may mediate the re- cation, shelter, fuel, clothing, and protection than those grown at ambient levels (78). sulting health impacts. If a change in a natu- from natural hazards and infectious disease. Modeling studies caution that warmer days ral system leads to an altered risk of exposure A majority of people are able to make this will lead to higher concentrations of ground- to disease, how will local populations respond transition and reap the benefits noted by level ozone and smog, which cause sickness to this new risk? If wildlife or fisheries are no Smith and Ezzati. However, the poorest and and death from respiratory and cardiac dis- longer sufficient to support harvest for hu- least entitled may fail to make the transition ease (79). Natural hazards including droughts, man nutrition, what and how will people successfully, unable to access either the floods, tropical cyclones, forest fires, and heat substitute for this loss and what will be the engineered infrastructure or markets (Fig. waves are projected to become more frequent nutritional value of this substitution? If de- 2). They are left with degraded natural sys- (80). Studies predict multiple impacts of cli- forestation leads to increased malaria expo- tems but little with which to replace them. matic disruption on food production and food sure, will local populations have access to bed In urban areas, these are slum dwellers security, as well as impacts on access to nets or antimalarial medications? Under- without access to municipal water and sewage freshwater (81–83). Several reports have standing these and other human responses is services, safe housing,healthcare,orother

Myers et al. PNAS | November 19, 2013 | vol. 110 | no. 47 | 18755 Downloaded by guest on October 1, 2021 CHANGES IN LAND USE AND COVER Deforestation, dams and irrigation, agricultural extension and intensification, livestock management, urbanization, THRESHOLD F LITY OR R road construction ABI ESO ER UR LN CE VU ED ECOS MAG YSTEM CO G DA S N IN LLY ERV S CH A IC TR A OC ES A O L NVIRONM W IN R E M E ENTA I P C FRO L C TH T P LA HA A P ED N R E CT G E T R E Y LEARNED O E G O T B R B I N O ED CU Y O N A R T LT N P EC U IN A C T R N E A F L IS O TY N T PR L R O N R FE O / I P A T L A DETERIORATION OF O S EC Y G T I N T S IC S D T L A T O N I P P E R O ECOSYSTEM SERVICES L A IO O T U L O T B U T R A P E C U A H A RESOURCE SCARCITY P L U R L T T P L M L O U N U Provision of nutrition, safe U A O P P A I P T R N E P L

O I I E Land degradation, C O O E NEGATIVE water, clean air, protection P P H D O N /

water scarcity, deforestation, E

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HEALTH E

wildlife population declines A

regulation of infectious E

OUTCOMES O

I Fig. 1. Schematic of the complex relationships

O R diseases, and maintenance S

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E S man health. Drivers of global environmental change (e.g., land-use change, resource scarcity, or climate change) can directly pose health risks or impair ecosystem services that subsequently inﬂuence health. Population level vulnerability, however, will be CLIMATE CHANGE modiﬁed by multiple layers of social or infrastructure Warming temperatures, elevated barriers that can buffer or eliminate risks associated carbon dioxide, more extreme storms, hydrologic extremes, with these exposures. Together, all components must sea-level rise be considered to achieve realistic assessments of insulating layers population vulnerability.

critical services. In rural areas, they are the that research into the health effects of eco- their ability to replace these services with remote and poor who are challenged with, system alteration should be targeted at them. engineered infrastructure, markets, or phi- for example, dwindling marine and terrestrial Another way to conceptualize these health lanthropy. The people who are most impacted wildlife populations and other wild species impacts is illustrated in Fig. 1. A combination by changes in the function of natural systems, relied on for food. They experience degraded of anthropogenic environmental changes in- therefore, are those who are geographically soils, fresh water resources, and forests and cluding changes in land use and cover, re- located in areas of greatest change and who generally diminished ecosystem services from source availability, and climate interact to have the fewest resources to insulate them- the natural systems within which they live. alter the quality of ecosystem services avail- selves from these changes through markets or Wesuspectthatthispopulationofroughlya able to local populations. The vulnerability infrastructure. As a result, they follow the billion people living in absolute poverty with of a population to these changes depends on lower arrow in Fig. 2, whereas others navigate little access to improved water or sanitation the extent to which they are relying on these the transition with more success. and frequently experiencing undernutrition services, how close they are to thresholds That said, people in wealthier societies will are most susceptible to the health impacts of whereby further reductions in services have not be immune to changes in exposure to the quiet erosion of natural infrastructure and immediate impacts on their well-being, and infectious disease, the impacts of sea level

Fig. 2. Hypothetical ecological transition for a ﬁc- tional population. In this schematic, the population moves from a state (a) in which people rely primarily on natural systems for health-related ecosystem services to a state (c) where they become reliant on engineered infrastructure and markets for these services while ecological systems get degraded over time. Over the course of this transition (b), there are numerous society-level mediating inﬂuences that are likely to change the differential vulnerabilities and health status of members of the population. These include equity of income distribution, type and strength of governance, philanthropic safety nets, characteristics of the natural environment etc. It is also likely that the health implications of such a transition will be different for different dimensions of health.

18756 | www.pnas.org/cgi/doi/10.1073/pnas.1218656110 Myers et al. Downloaded by guest on October 1, 2021 rise, more extreme storms, and other natural the health impacts associated with these types We are confident, however, that changes in PERSPECTIVE hazards associated with climate change or the of environmental change are not distinct the structure and function of natural systems indirect effects of large-scale population dis- health outcomes but contributions to health arelikelytobroadlyimpactmanyofthemost placement that are likely to follow the break- outcomes whose causes are multifactorial important public health risks we face globally. down of ecosystem services. (88).Wemustask:howmuchofthemalaria These changes are significant drivers in the in the Brazilian Amazon is a result of defor- emergence, distribution, and transmission of How Big a Public Health Problem Is the estation, how much of the iron deficiency numerous infectious diseases. Recent work, Degradation of Natural Systems? in Madagascar is due to wildlife population for example, highlights the large burden as- In public health, this sort of question is best declines, and how much of the cardiopul- sociated with zoonotic diseases and the sig- answered using burden of disease assessment, monary disease in Singapore is due to forest nificant role that land-use change and re- which relies, for its metric, on the disability fires in Indonesia? These are tractable ques- source scarcity play in driving the emergence adjusted life-year (DALY). By estimating, for tions, but challenging, and they have not yet and transmission of these diseases (90). A a particular health threat, the amount of as- been answered. second example is the recent finding that sociated morbidity and mortality for differ- A third challenge is that many of the rela- Cryptosporidium infection is the second ent demographic groups within a population tionships we are interested in involve the loss leading cause of moderate to severe diarrhea and adjusting for the level of disability as- of a protective service as opposed to the in infants in the developing world (91). Di- sociated with nonfatal outcomes, it is pos- presence of a risk. Viewed through a burden arrheal disease accounts for 1 in 10 deaths in fi sible to represent the burden of any public of disease lens, the burden is, paradoxically, children under the age of ve and causes health threat using this metric. The advan- generated by the loss of a protection not the 800,000 deaths annually (91). This pathogen tage of such an approach is that it allows presence of an exposure. As a result, we are is found ubiquitously in cattle (92), and out- comparison across widely different health concerned with calculating the “disease aver- breaks have been associated with both land- threats (e.g., alcoholism vs. measles) to as- ted” that is associated with a natural system in usechangeandextremeprecipitation(76, sess their relative importance for a particular a particular state. For example, as overfishing 93). Other causes of childhood diarrhea are population or globally. continues around the world, we expect to see also likely to be sensitive to changes in land One widely publicized assessment of the additional burdens of disease from malnutri- use and precipitation patterns. global burden of disease associated with tion among poor coastal peoples. The ques- Changes in the state of natural systems are changes in the environment concluded that tion is not just the degree of protein, calorie, also likely to exacerbate both undernutrition roughly one quarter of the global burden of and micronutrient deficiencies that remain and micronutrient deficiencies caused today, disease can be attributed to environmental large contributors to the global burden of but how much will be seen in the future if changes (87). This effort and many associated disease. Wildlife population declines are im- sustainable fisheries management remains efforts to quantify disease burdens associated pacting both macro- and micronutrient nu- largely elusive? As we expressed earlier, the with environmental risk factors have, how- trition for many populations, whereas climate burden of ecosystem alteration may be dis- ever, had a very different focus than that of change is expected to reduce the iron, zinc, proportionately experienced by future gen- this paper. The environment of concern in and protein content of grains that are a criti- erations. Recent evidence that global per these efforts has primarily been the household cal source of these nutrients for large seg- environment with unsafe water, sanitation, capita burden of disease is in decline along mentsofthehumanpopulation(94–97). In and hygiene, indoor air pollution, and out- with death and disability in children under fi fi combination, iron and zinc de ciency have door air pollution comprising the bulk of the ve is encouraging (89); our concern is that been estimated by the World Health Organi- risks. In addition, they included some of growing resource scarcity, changes in land use zation to cause 63 million life-years to be lost the classic elements of environmental health: and cover, climate change effects, and alter- annually (98, 99). The combination of arable exposures associated with occupations, radia- ations to a range of ecosystem services are in land degradation, increasing water scarcity, tion, or heavy metals. Such analyses are enor- danger of countering or even reversing these and climatic disruption is expected to reduce mously valuable in helping public health trends in the future. agricultural yields at thesametimethathu- practitioners determine the relative gains that Finally, the interactions between environ- manity will need to roughly double global can be achieved in the overall health of a mental changes at the population level and food production to keep up with demand population by modifying these aspects of the the mediating effect of human responses are (100, 101). These environmental headwinds environment. However, they explicitly ex- enormously complex. In sub-Saharan Africa, are almost certain to produce regional, if not cluded “natural environments or ecosystems for example, how will the combination of global, food shortages. that cannot reasonably be modified” as be- altered land cover, water scarcity, wildlife Even heart disease, which makes up an yond their scope and do not, therefore, pro- population declines, and climate change ef- increasing share of the global burden of dis- vide us guidance on the relative importance of fects interact to affect the quality and quantity ease (89), is susceptible to changes in the ecosystem change to human health (87). of food and water available? How will climatic functioning of natural systems. For example, Quantifying the disease burden associated changes and altered access to food and water large percentages of the global production of with changes in the structure and function of contribute to population displacement? How nutrients like folic acid and vitamin E come natural systems presents several challenges. will population displacement alter the in- from crops dependent on animal polli- The firstisthatourunderstandingofthe cidence of infectious disease and malnutrition nators, and dietary intake of these nutrients health impacts remains incomplete. As out- among the displaced, and to what extent will is associated with reduced risk of heart lined above, there are many systems and people moving into places where they are not disease (66). At the same time, rising con- dimensions of health where much more work welcome generate civil strife? These types of centrations of atmospheric CO2 have been needstobedonebeforewewillfullyun- interactions will contribute to future burdens shown to lower the protein content in the derstand the health implications of ecosystem of disease but, at our current level of un- major grains (97), and the resulting sub- change. A second challenge is that most of derstanding, are impossible to quantify. stitution of dietary carbohydrate for dietary

Myers et al. PNAS | November 19, 2013 | vol. 110 | no. 47 | 18757 Downloaded by guest on October 1, 2021 protein has been shown to increase the risk be expected to affect transmission of other calories produced for human consumption of coronary heart disease (102). burdensome diseases and how generalizable (67) but more specific work would allow us Changes to Earth’snaturalsystemsaffect these relationships are across different spatial to quantify the importance of pollination the quality of the water we drink and the air scales.Applyingmethodsthatarealready services for both micro- and macronutrition we breathe by multiple mechanisms and im- developed, investigators could characterize for particular populations around the world pact our vulnerability and exposure to natural these relationships more completely, with and to model the health implications of pol- hazards. We know that these changes are theresultingknowledgebaseinforming linator declines in those locations. pervasive, affecting nearly every natural sys- natural resource management much more There is much to learn about how different tem on Earth and that they are accelerating. meaningfully. animal husbandry practices, land uses, and They impact both directly and indirectly most In disease ecology, much of the founda- incursions into wildlife habitat affect the de- ofthediseasesthatmakeupthemajorityof tional work has been done using infectious velopment and transmission of new zoonotic the global burden of disease. For the reasons disease systems that are associated with rel- infections (105). This understanding will be outlined above, it is not yet possible to quan- atively small burdens of disease. We would important to the development of more ef- tify the burden of disease associated with the benefit from greater understanding of the fective surveillance approaches. In the area of disruption of these natural systems to the complex ecology of infectious diseases asso- climate change, there are many open ques- same degree that has been accomplished with ciated with very large global burdens such as tions that should be a priority, including the other types of environmental health risks. We malaria, diarrhea, influenza, schistosomiasis, numerous and interacting impacts of climate suspect, however, that the health burden as- dengue, Chagas disease, and leishmaniasis. change on food production and availability sociated with ecosystem alterations will be on In addition, as outlined above, there is im- and the impacts of climatic disruption on the a par with those other types of environmental portant work to do to characterize whether timing, quantity, and quality of water available health risks which were found to account for there are differences between those organisms for different populations. Determining the fi roughly one quarter of the global burden of that are rst removed from a community effects of climate change on the geographic disease (87). during disturbance and those which are left distribution of infectious diseases is another behind with respect to their ability to transmit important area of active research. Of course, Moving Forward infectious diseases. Such differences might this is not an exhaustive list but is meant to Environmental health has always been a help to explain whether there are general be illustrative. pragmatic discipline focused on identifying principles like the dilution effect that can and quantifying threats to human health in be expected to hold up across different sys- Address the Limitations. As we set about the environment so that these threats can be tems and diseases. Finally, the field would filling the gaps in our understanding, we also addressed. Removing lead from gasoline benefit from more studies that look at the need to address the limitations outlined and the Clean Air Act and Clean Water Act impacts of disturbance or management in- above. Research efforts that explore multiple in the United States are prominent exam- terventions on the ecology of multiple dis- health outcomes from a particular ecosystem ples. In the relatively new branch of envi- eases simultaneously. For example, recent alteration may generate more useful insights ronmental health focused on the health work in Uganda shows how forest fragmen- for policy and practice than studies focused impacts of changes in the structure and tation and disturbance alter exposure among on a single health outcome. New approaches function of natural systems, we believe that both humans and apes to a variety of different that allow us to anticipate the health impacts of we need a similarly pragmatic focus. Al- infectious disease agents (103). multiple, interacting environmental changes though our understanding of the health We still have little understanding of the including resource scarcity, land-use change, impacts of ecosystem alteration in some role that marine and terrestrial wildlife spe- and climate change should, in many instances, areas is already adequate to inform policy cies play in providing both macro- and mi- provide more realistic estimates than analyses decisions—the need to anticipate changes cronutrients for the many people who, for that look at a particular change in isolation. in vector-borne disease exposure associated numerous reasons, do not have access to Research in the Brazilian Amazon exploring with dams and irrigation projects, for these nutrients through alternative sources. multiple health outcomes associated with a example—our understanding remains too In a few populations, careful work comparing combination of climate change and defor- patchy to meaningfully inform policy or dietary survey data, biomarkers of nutrition, estation is one example of such work (106). resource management decisions in many food composition analysis, and anthropom- Expandingresearchtofactorinhumanre- fi systems. We propose the following steps to etry is allowing quanti cation of the nutri- sponses and adaptations to environmental generate a more robust and useful under- tional importance of access to wildlife in the changes will also provide more realistic esti- standing of these relationships. diet (68). This work might fruitfully be ex- mates of real world impacts of ecosystem al- tended to other systems and populations to terations on human health, and some work Fill the Gaps. Many of the relationships assess how wildlife management, including has been achieved in this area (107, 108). Fi- that have been explored in the studies out- marine conservation (104), impacts the nu- nally, we will reach more clarity by being very lined above remain incompletely character- tritional status of local populations depen- specific about whose health is being studied ized. Snapshots of particular disease/land dent upon these species for key nutrients. within a population or by explicitly disaggre- cover relationships in specific locations (e.g., Beyond the nutritional provisioning ser- gating different segments of a population to deforestation and schistosomiasis in Came- vice of wildlife in the diet, there is a great deal look at differential impacts. roon) are compelling evidence that land cover of work to be done to characterize the health In addition to filling gaps in our under- changes can alter infectious disease trans- values of other ecosystem services and the standing and addressing several limitations, mission, but they fall short of allowing resource impacts on health of changes in the condition we propose two additional approaches that managers and policy makers to anticipate the of these systems. For example, pollination could help to guide future work. full health implications of their decisions. We services have been shown to underpin the Respond to specific policy needs. Much of the need to understand how these changes might production of roughly one third of global existing research appears to have been driven

18758 | www.pnas.org/cgi/doi/10.1073/pnas.1218656110 Myers et al. Downloaded by guest on October 1, 2021 by scientific curiosity more than pragmatic would allow us to functionally define the key Conclusion PERSPECTIVE questions about how to manage natural components of natural systems that support Human activity is transforming Earth’snat- systems to optimize health and environ- human health and to predict the health im- ural systems in ways that are profound, per- mental outcomes. Only after obtaining re- pacts of incremental changes in those com- vasive, and accelerating. This transformation sults do scientific teams typically work to fi ponents. For example, the use of re as a is generating a suite of health impacts that apply their findings to policy. We propose land-clearing approach in Southeast Asia is remain, in many instances, poorly charac- increased emphasis on policy-driven research. a major threat to biodiversity in the region terized. However, ample evidence exists For example, what are the likely impacts and is also responsible for significant partic- ’ that nearly every dimension of human of recent changes in Brazil s forest code on ulate air pollution exposures for downwind malaria rates in Amazonian states (109, 110)? populations in Indonesia, Singapore, and health is being affected, and it is likely that The answer to this exciting research question, the disease burden associated with these fi Malaysia. Estimating the emissions associated which would require eld experiments and with these fires and modeling their chemical aggregate ecosystem alterations is large modeling to unravel, would almost in- evolution as they are transported through and growing. We propose a more system- evitably inform refinementsofthispolicy. space and time to reach downwind popula- atic and comprehensive approach to un- Scientific efforts in biodiversity conserva- tions will allow policy makers to understand tion, ecosystem services, and many other derstanding the health impacts of ecosys- how fires associated with particular geogra- policy-relevant fields also tend to proceed tem alteration to better inform decision from basic research to policy application, phies, land cover types, or land uses are af- making in the land-use planning, environ- fecting morbidity and mortality (primarily and we believe that a basic reversal of ap- mental conservation, and public health from cardiorespiratory disease) for regional proach would increase the value of research policy realms. results to society. Accomplishing this shift populations. Such work will allow land-use from curiosity-driven to policy-driven re- planners to factor in the public health impli- ACKNOWLEDGMENTS. We acknowledge support cations of the decisions they are making in a fromtheentireHealth&Ecosystems:AnalysisofLink- search will require a parallel culture shift in ages (HEAL) consortium in framing many of the issues the scientific disciplines such that incentives way that has been elusive to date. This careful discussed in this article. In particular, we thank the in the form of promotions, funding, and quantification of specific health impacts as following individuals for valuable feedback on earlier a function of changes in environmental con- versions of this manuscript: Stacy Jupiter, Carter success in publishing are consistent with Ingram, Arlyne Johnson, Mike Mascia, David Wilkie, this emphasis. dition is critical to moving away from an ab- and Ilana Brito. We also thank Damien Joly for assis- Build production functions. stract discussion about the importance of tance in preparing Fig. 2 and Kellie Nault for assis- In wide use in the tance in preparing Fig. 1. This work was supported industrial and agricultural sciences, produc- natural systems to human health, and toward by The Gordon and Betty Moore Foundation and tion functions relate the amounts and quali- concrete tools that allow policy makers and The Rockefeller Foundation as part of the Health & Ecosystems: Analysis of Linkages (HEAL) program. ties of inputs to the amounts of particular resource managers to quantify the health Support was also received from the Bill and Melinda outputs in a system. Adapting this approach implications of the decisions they make. Gates Foundation.

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