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Soil ecosystem services and human health
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Current Opinion in
Environmental Science & Health
Soil ecosystem services and human health Eric C. Brevik1, Lily Pereg2, Joshua J. Steffan1,3 and Lynn C. Burgess1 Abstract
The impact of soils on human health is well-documented, and the ecosystem services (ES) provided by soils are important to human health. However, previous works on soils and human health have not approached the topic from a soil ES perspective. This paper provides examples of ways that soil ES support human health. Provisioning services ensure a plentiful supply of nutritious food products, building supplies that allow the construction of housing that protects human health from inclement weather, fibers for clothing that aid in body heat regulation, and fuel to heat houses during cold weather. Several of these relationships, like the provisioning of shelter and heat, have not been previously explored in the soils and human health literature. Regulating services relevant to human health include pathogen regulation and greenhouse gas cycling. Cultural services are important in healing, stress reduction, and recreation. The examples presented in this paper demonstrate the influence that soil ES have on human health and that taking an ES approach when considering soils and human health has the potential to identify areas that need further investigation. Addresses 1 Department of Natural Sciences, Dickinson State University, Dickinson, ND, USA 2 School of Science and Technology, University of New England, Armidale, NSW, 2351, Australia 3 Department of Agriculture and Technical Studies, Dickinson State University, Dickinson, ND, USA Corresponding author: Brevik, Eric C. (Eric.Brevik@dickinsonstate. edu)
Current Opinion in Environmental Science & Health 2018, 5:87–92 This review comes from a themed issue on Sustainable soil management and land restoration Edited by Paulo Pereira and Juan F. Martínez-Murillo
includes positive influences such as the supply of essential nutrients to produce nutritious food products for the human diet, water purification services, and a source of medications, especially antibiotics. However, soil can also negatively influence human health due to exposure to hazardous substances and pathogens within the soil. Soils are not often recognized in the literature as influencing human health through their production of products such as wood (for lumber or timber) and clay (used for brick) that are important in the construction of shelters that provide refuge from inclement weather, fibers such as cotton that provide clothing for body temperature regulation, and fuel sources such as wood that provide heat. Soil degradation decreases the ability of a soil to support human health and efforts to end or reverse degradation improve that ability [6,7]. Studies investigating the natural services provided by soils go back to the 1960s, and by the 1970s and 1980s soil scientists were classifying these services into soil functions [8]. However, including soils in ecosystem services (ES) assessments was rare until the 2000s as broad, general approaches to evaluating ES were favored [8,9]. General interest in ES increased after 2000 and again after 2005 [9], with an increasing focus on the contributions of soils to ES after about 2009 [8]. The most commonly used ES classifications are elucidated by the Millennium Ecosystem Assessment (MEA), the Economics of Ecosystems and Biodiversity, the Common Classification of Ecosystem Services (CICES), and OpenNESS [10]. The CICES system was developed with the MEA [11] as its starting point but has been constantly updated over time [12]. The CICES classification divides ES into three categories: 1) provisioning, 2) regulation and maintenance, and 3) cultural [12]. The CICES classification will be used for the discussion that follows.
For a complete overview see the Issue and the Editorial
https://doi.org/10.1016/j.coesh.2018.07.003 2468-5844/© 2018 Elsevier B.V. All rights reserved.
Keywords Soil and human health, Provisioning services, Regulating services, Cultural services, CICES.
Introduction The profound impact of soils on human health is well documented [1e5], and soils are now recognized as influencing human health in a number of ways. This
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A number of papers have given general overviews of ES and human health in recent years [e.g., 13, 14]. There have also been reviews looking at more specific issues, such as the links between ES, human health, and biodiversity [15], green infrastructure [16], social depravation [17], oceans [18], and climate change [19]. In fact, the ES concept was originally developed to assess the effects of lost ecosystem function and biodiversity on human well-being [20]. Given the information above, soil ES should be important in supporting human health. However, few previous works on soils and human health have approached the topic from an ES perspective. Keith et al. [21] connected ecosystem services to the One Health initiative through soil Current Opinion in Environmental Science & Health 2018, 5:87–92
88 Sustainable soil management and land restoration
stewardship, however, their evaluation very specifically addressed One Health and did not step through links between individual soil ecosystem services and human health. Therefore, the objective of this paper is to review examples of soil ES that are important to human health and point out the need for studies into soils and human health that take a soil ES approach.
Provisioning services Provisioning services refer to all nutritional, nonnutritional material, and energetic outputs from living systems as well as abiotic outputs [12]. While this gives a fundamental description of provisioning services, at times the MEA explanations are more clear and straightforward than the CICES definitions. The MEA defines provisioning services as products that soil ES make available for human use [11]. These include nutrients, water and other materials that are important for the growth and production of food and fiber products, fuelwood, potable drinking water, medicines, and genetic resources [11]. The production of large quantities of quality food is one area of soils and human health that has received much attention [22] (Figure 1). The links between food production, particularly plant-based food products and soils, are straightforward and simple to understand and people tend to focus on fairly obvious health connections [23]. Many of the nutrients that are important to human health originate in soil. These
nutrients are supplied to plants as they grow in soil, and are then passed on to humans who consume plant material directly or the meat of animals that fed on those plants [24]. In some cases, organisms can improve human health by enhancing plant production and be a source of food themselves. Some of the most sought after edible mushrooms belong to the mycorrhizal fungi group [25], which provide a food source and help plants, ranging from crops to trees, obtain needed soil-derived nutrients [26]. The importance of building materials, fiber, and fuel that are provided by soils in the promotion of human health have received much less discussion in the soils and human health literature than other provisioning service topics. Building materials such as wood (for lumber or timber) and clay (for brick) are important in the construction of homes and other buildings that provide shelter from storms and allow the creation of controlled spaces where temperatures can be regulated. Plant fibers such as cotton, flax, and hemp are important to make clothing; approximately 68% of women’s and 85% of men’s clothing in the USA contains cotton [27]. Over 5300 people are estimated to have died in the USA between 2004 and 2013 due to extreme weather events, with more than 1400 of those deaths due to temperature extremes [28]. To combat extreme cold, sheltered spaces are heated and wood is the
Figure 1
The production of large quantities of quality food (top), a provisioning service, is one of the most studied and recognized links between soils and human health. The importance of the provisioning services supplied by soils in the production of products such wood (bottom), which is important as a building material for shelter against extreme weather and fuel for a source of heat to combat extreme cold, is often overlooked when discussing soil-human health connections. Photos by E.C. Brevik. Current Opinion in Environmental Science & Health 2018, 5:87–92
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Soil ecosystem services and human health Brevik et al.
primary heating fuel for about 2% of households in the USA [29]. While this percentage is typical of developed countries, fuelwood represents about 7% of energy consumption world-wide and 15% in developing counties [30]. These numbers were much higher prior to the 19th century when wood was humanity’s primary energy source [31]. Fuel for the appropriate cooking of foods is also an important part of preventing foodborne disease [32]. Through their provision of shelter, clothing, and fuel to regulate the living environment, cook food, etc., products supplied by soils contribute to improved human health (Figure 1). Soil properties and functions are very important in provisioning services. The nutritional value of plants that form the base of the food chain, the growth of woody plants for burning and building (Figure 1), and recreational forests (Figure 2) are all dependent on soil structure, biodiversity, and the balance of nutrients in the soil. Most of the nutrients required by plants for new growth are provided by decomposition of dead organic matter and nutrient recycling. This is provided by soil biota and the fulfillment of the full scale of soil biological functions is highly dependent on maintaining high biodiversity [33]. Surface soils are fertilized with litter and feces from temporary soil residents such as burrowing mammals. Organic matter can be dispersed and mechanically decomposed by macro- and mesofauna, such as ants, termites, millipedes, earthworms and snails [34]. Carbon is transformed by decomposition of OM by meso- and microfauna, such as protozoa, nematodes and mites. A variety of heterotrophic soil microorganisms (fungi and bacteria) degrade OM and other microbes fix carbon and nitrogen. The nutrients released (e.g., N, P, S) are assimilated by soil microbes and new vegetation [35]. This includes the crops, forages, and trees important to human health.
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Regulating services Regulating services refer to ways that living organisms can mediate or moderate the environment and affect human health, safety or comfort, including abiotic equivalents [12]. The soil system plays a role in the regulation of several ecosystem processes, including air quality maintenance, climate regulation, water regulation, erosion control, water purification and waste treatment, promotion of plant growth and regulation of diseases [2,36e38]. Two brief examples will be discussed here. Soils are host to a wide range of microorganisms and viruses, some of which are pathogenic. Some of these microorganisms and viruses are naturally found in soils while others have been anthropogenically introduced [39]. Pathogenic organisms can be incorporated into soils in a number of ways, including the application of night soil, sewage sludge, municipal wastewater, or animal wastes to soils as nutrient sources or through the use of septic systems to dispose of human wastes. The environmental conditions an organism encounters when introduced into soil largely determine the survival time of that organism in the soil system. Many pathogens can be readily sorbed to soil particles or filtered out of liquid mixtures by clay-rich soils. The movements of other organisms are restricted by unsaturated flow due to greater soil-to-pathogen contact that traps the organism. On the other hand, high flow rates through large soil pores tends to favor rapid pathogen movement through soils [40]. Soil moisture status, temperature, pH, organic matter content, and exposure to sunlight all influence pathogen survival [39]. Pathogen populations in the soil are also controlled by predators and parasites, such as protozoa and bacteriophages as well as by antagonistic microbes and competition for space in a suitable ecological niche. Therefore, diverse populations of organisms help to limit pathogen numbers [41]. Because of the ability of soils to
Figure 2
Exposure to attractive natural landscapes, which are underpinned by soils, has been shown to produce positive health benefits, and soils are an important consideration when properly planning recreational features such as hiking trails. These are examples of cultural services provided by soil. Photo by E.C. Brevik. www.sciencedirect.com
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regulate pathogens, well designed, properly maintained and functioning on-site sewage treatment systems are highly effective at reducing water-borne diseases in areas with low population densities [42]. Soil biota are also involved in decontaminating the environment from toxic waste by phytoremediation and microbial bioremediation [43,44], again highlighting the importance of soil biodiversity to human health. In fact, the use of soils to address groundwater contamination issues has been one of the fastest growing areas of soil science in recent years [45]. Finally, soil biodiversity is important for maintaining soil physical structure and preventing soil degradation. Fungal hyphae networks, together with microbial glues and slimes produced by OM degradation, bind primary inorganic particles into soil aggregates and plant roots stabilize loose soil [46]. This is important in soil conservation and also reduces dust and thus the spread of pathogens to humans and animals [2]. Links to the soil ES water purification and waste treatment and regulation of diseases can be seen in this example. Soils are intimately linked to the cycling of several greenhouse gases, including CO2 (Figure 3), CH4, and N2O, meaning these gases fall within the regulating services provided by soils. Human management of soils can either increase or decrease the levels of carbon and nitrogen based gases in the atmosphere [38], and the presence of these gases may cause a number of health
problems for humans [2]. Human management of soils can influence the balance between C and N sequestered in and the emissions of C and N containing gases from soils. The type of tillage used to manage agricultural fields, the number of machine passes (which influences soil organic matter decomposition rates and fuel consumption), crop rotations, use of cover crops, types of fertilizer used, types of organic residues applied and whether they are incorporated into the soil or left on the soil surface, and the length of the flooded period in rice paddies are all management decisions that influence the C and N balances in agricultural soils and represent direct interactions between soils and atmospheric greenhouse gas levels [38,47]. Here too the importance of soil biodiversity and the presence of varied microbial functional groups that are involved in nutrient cycling is highlighted [33]. The quality of food is also affected. A meta-analysis demonstrated that increased atmospheric CO2 decreases overall mineral concentrations and increases the ratio of carbohydrates to minerals in 130 varieties of plants, increasing the likelihood of hidden hunger and obesity [48]. Links to the ES climate regulation can be seen in this example.
Cultural services Cultural services refer to the non-material, and normally non-rival and non-consumptive outputs of ecosystems (biotic and abiotic) that affect the physical and mental
Figure 3
Soil is an important part of several cycles, including the carbon cycle. This diagram provides a simplified summary of the role soil plays in the carbon cycle, which is in turn important in regulating planetary temperatures. Soil plays an important role in human health through its influence on climate, a regulating service.
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Soil ecosystem services and human health Brevik et al.
states of people [12]. The MEA defined these as nonmaterial benefits people obtain from ecosystems through spiritual enrichment, cognitive development, reflection, recreation, and aesthetic experiences [11]. The horticultural community has conducted studies that demonstrate exposure to plants speeds the healing process for patients after surgery [49], walking through a garden helps restore mental clarity [50], and stress reduction and restoration from mental fatigue have been documented for people exposed to attractive landscapes [51,52] (Figure 2). Care farming, where commercial farms and agricultural landscapes are used to promote mental and physical health during the course of normal farming activity [53], has also been shown to improve mental, physical, and social health [53e55]. In each of these cases, soils are the medium within which the garden plants grow or agriculture is carried out. In this context, soils have an indirect benefit on human health. However, additional direct benefits have also been examined; for example, gardeners may respond positively to working with soil [56]. Soils are also important in recreation. The most direct link is probably gardening, where the gardener works with soil. Gardening has been shown to improve mental and physical health as well as encourage healthy eating through increased consumption of fresh fruits and vegetables [57,58]. While this is an indirect health link, Hanyu et al. [59] have documented exposure to healthy soils leading to a state of physiological and mental relaxation and reduced stress. Recreational activities such as hiking, camping, and biking also improve mental and physical health [60,61], and soils information is important in planning trails and campsites to maximize the recreational experience (Figure 2). The US National Cooperative Soil Survey has included information on the suitability of soils for a variety of recreational activities in their soil survey reports since the 1960s [62]. Therefore, soils contribute both directly and indirectly to the promotion of human health through cultural services.
Concluding statements It is important to note that the issues discussed in this paper are examples, not comprehensive discussions of the ways that soil ES influence human health. The space available here is too short for a comprehensive discussion. However, this paper does point out clear examples of ways that human health is linked to soil ES. Furthermore, it demonstrates that taking an ES approach when considering soils and human health has the potential to identify areas that need further investigation, such as the influence of soils on human health through the provisioning of building materials, fiber, and fuel. Lastly, the importance of avoiding or correcting soil degradation to provide the healthy soils necessary to maximize soil ES that support human health cannot be overlooked. To this point the soils and human health literature has not focused on connections between soil ES and human health. An increased focus on this area in the future would be beneficial. www.sciencedirect.com
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Conflict of interest statement Nothing declared.
Acknowledgements E. Brevik and J. Steffan were partially supported by the National Science Foundation under Grant Number IIA-1355466 during this project.
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ScienceDirect
Current Opinion in
Environmental Science & Health
Soil ecosystem services and human health Eric C. Brevik1, Lily Pereg2, Joshua J. Steffan1,3 and Lynn C. Burgess1 Abstract
The impact of soils on human health is well-documented, and the ecosystem services (ES) provided by soils are important to human health. However, previous works on soils and human health have not approached the topic from a soil ES perspective. This paper provides examples of ways that soil ES support human health. Provisioning services ensure a plentiful supply of nutritious food products, building supplies that allow the construction of housing that protects human health from inclement weather, fibers for clothing that aid in body heat regulation, and fuel to heat houses during cold weather. Several of these relationships, like the provisioning of shelter and heat, have not been previously explored in the soils and human health literature. Regulating services relevant to human health include pathogen regulation and greenhouse gas cycling. Cultural services are important in healing, stress reduction, and recreation. The examples presented in this paper demonstrate the influence that soil ES have on human health and that taking an ES approach when considering soils and human health has the potential to identify areas that need further investigation. Addresses 1 Department of Natural Sciences, Dickinson State University, Dickinson, ND, USA 2 School of Science and Technology, University of New England, Armidale, NSW, 2351, Australia 3 Department of Agriculture and Technical Studies, Dickinson State University, Dickinson, ND, USA Corresponding author: Brevik, Eric C. (Eric.Brevik@dickinsonstate. edu)
Current Opinion in Environmental Science & Health 2018, 5:87–92 This review comes from a themed issue on Sustainable soil management and land restoration Edited by Paulo Pereira and Juan F. Martínez-Murillo
includes positive influences such as the supply of essential nutrients to produce nutritious food products for the human diet, water purification services, and a source of medications, especially antibiotics. However, soil can also negatively influence human health due to exposure to hazardous substances and pathogens within the soil. Soils are not often recognized in the literature as influencing human health through their production of products such as wood (for lumber or timber) and clay (used for brick) that are important in the construction of shelters that provide refuge from inclement weather, fibers such as cotton that provide clothing for body temperature regulation, and fuel sources such as wood that provide heat. Soil degradation decreases the ability of a soil to support human health and efforts to end or reverse degradation improve that ability [6,7]. Studies investigating the natural services provided by soils go back to the 1960s, and by the 1970s and 1980s soil scientists were classifying these services into soil functions [8]. However, including soils in ecosystem services (ES) assessments was rare until the 2000s as broad, general approaches to evaluating ES were favored [8,9]. General interest in ES increased after 2000 and again after 2005 [9], with an increasing focus on the contributions of soils to ES after about 2009 [8]. The most commonly used ES classifications are elucidated by the Millennium Ecosystem Assessment (MEA), the Economics of Ecosystems and Biodiversity, the Common Classification of Ecosystem Services (CICES), and OpenNESS [10]. The CICES system was developed with the MEA [11] as its starting point but has been constantly updated over time [12]. The CICES classification divides ES into three categories: 1) provisioning, 2) regulation and maintenance, and 3) cultural [12]. The CICES classification will be used for the discussion that follows.
For a complete overview see the Issue and the Editorial
https://doi.org/10.1016/j.coesh.2018.07.003 2468-5844/© 2018 Elsevier B.V. All rights reserved.
Keywords Soil and human health, Provisioning services, Regulating services, Cultural services, CICES.
Introduction The profound impact of soils on human health is well documented [1e5], and soils are now recognized as influencing human health in a number of ways. This
www.sciencedirect.com
A number of papers have given general overviews of ES and human health in recent years [e.g., 13, 14]. There have also been reviews looking at more specific issues, such as the links between ES, human health, and biodiversity [15], green infrastructure [16], social depravation [17], oceans [18], and climate change [19]. In fact, the ES concept was originally developed to assess the effects of lost ecosystem function and biodiversity on human well-being [20]. Given the information above, soil ES should be important in supporting human health. However, few previous works on soils and human health have approached the topic from an ES perspective. Keith et al. [21] connected ecosystem services to the One Health initiative through soil Current Opinion in Environmental Science & Health 2018, 5:87–92
88 Sustainable soil management and land restoration
stewardship, however, their evaluation very specifically addressed One Health and did not step through links between individual soil ecosystem services and human health. Therefore, the objective of this paper is to review examples of soil ES that are important to human health and point out the need for studies into soils and human health that take a soil ES approach.
Provisioning services Provisioning services refer to all nutritional, nonnutritional material, and energetic outputs from living systems as well as abiotic outputs [12]. While this gives a fundamental description of provisioning services, at times the MEA explanations are more clear and straightforward than the CICES definitions. The MEA defines provisioning services as products that soil ES make available for human use [11]. These include nutrients, water and other materials that are important for the growth and production of food and fiber products, fuelwood, potable drinking water, medicines, and genetic resources [11]. The production of large quantities of quality food is one area of soils and human health that has received much attention [22] (Figure 1). The links between food production, particularly plant-based food products and soils, are straightforward and simple to understand and people tend to focus on fairly obvious health connections [23]. Many of the nutrients that are important to human health originate in soil. These
nutrients are supplied to plants as they grow in soil, and are then passed on to humans who consume plant material directly or the meat of animals that fed on those plants [24]. In some cases, organisms can improve human health by enhancing plant production and be a source of food themselves. Some of the most sought after edible mushrooms belong to the mycorrhizal fungi group [25], which provide a food source and help plants, ranging from crops to trees, obtain needed soil-derived nutrients [26]. The importance of building materials, fiber, and fuel that are provided by soils in the promotion of human health have received much less discussion in the soils and human health literature than other provisioning service topics. Building materials such as wood (for lumber or timber) and clay (for brick) are important in the construction of homes and other buildings that provide shelter from storms and allow the creation of controlled spaces where temperatures can be regulated. Plant fibers such as cotton, flax, and hemp are important to make clothing; approximately 68% of women’s and 85% of men’s clothing in the USA contains cotton [27]. Over 5300 people are estimated to have died in the USA between 2004 and 2013 due to extreme weather events, with more than 1400 of those deaths due to temperature extremes [28]. To combat extreme cold, sheltered spaces are heated and wood is the
Figure 1
The production of large quantities of quality food (top), a provisioning service, is one of the most studied and recognized links between soils and human health. The importance of the provisioning services supplied by soils in the production of products such wood (bottom), which is important as a building material for shelter against extreme weather and fuel for a source of heat to combat extreme cold, is often overlooked when discussing soil-human health connections. Photos by E.C. Brevik. Current Opinion in Environmental Science & Health 2018, 5:87–92
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primary heating fuel for about 2% of households in the USA [29]. While this percentage is typical of developed countries, fuelwood represents about 7% of energy consumption world-wide and 15% in developing counties [30]. These numbers were much higher prior to the 19th century when wood was humanity’s primary energy source [31]. Fuel for the appropriate cooking of foods is also an important part of preventing foodborne disease [32]. Through their provision of shelter, clothing, and fuel to regulate the living environment, cook food, etc., products supplied by soils contribute to improved human health (Figure 1). Soil properties and functions are very important in provisioning services. The nutritional value of plants that form the base of the food chain, the growth of woody plants for burning and building (Figure 1), and recreational forests (Figure 2) are all dependent on soil structure, biodiversity, and the balance of nutrients in the soil. Most of the nutrients required by plants for new growth are provided by decomposition of dead organic matter and nutrient recycling. This is provided by soil biota and the fulfillment of the full scale of soil biological functions is highly dependent on maintaining high biodiversity [33]. Surface soils are fertilized with litter and feces from temporary soil residents such as burrowing mammals. Organic matter can be dispersed and mechanically decomposed by macro- and mesofauna, such as ants, termites, millipedes, earthworms and snails [34]. Carbon is transformed by decomposition of OM by meso- and microfauna, such as protozoa, nematodes and mites. A variety of heterotrophic soil microorganisms (fungi and bacteria) degrade OM and other microbes fix carbon and nitrogen. The nutrients released (e.g., N, P, S) are assimilated by soil microbes and new vegetation [35]. This includes the crops, forages, and trees important to human health.
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Regulating services Regulating services refer to ways that living organisms can mediate or moderate the environment and affect human health, safety or comfort, including abiotic equivalents [12]. The soil system plays a role in the regulation of several ecosystem processes, including air quality maintenance, climate regulation, water regulation, erosion control, water purification and waste treatment, promotion of plant growth and regulation of diseases [2,36e38]. Two brief examples will be discussed here. Soils are host to a wide range of microorganisms and viruses, some of which are pathogenic. Some of these microorganisms and viruses are naturally found in soils while others have been anthropogenically introduced [39]. Pathogenic organisms can be incorporated into soils in a number of ways, including the application of night soil, sewage sludge, municipal wastewater, or animal wastes to soils as nutrient sources or through the use of septic systems to dispose of human wastes. The environmental conditions an organism encounters when introduced into soil largely determine the survival time of that organism in the soil system. Many pathogens can be readily sorbed to soil particles or filtered out of liquid mixtures by clay-rich soils. The movements of other organisms are restricted by unsaturated flow due to greater soil-to-pathogen contact that traps the organism. On the other hand, high flow rates through large soil pores tends to favor rapid pathogen movement through soils [40]. Soil moisture status, temperature, pH, organic matter content, and exposure to sunlight all influence pathogen survival [39]. Pathogen populations in the soil are also controlled by predators and parasites, such as protozoa and bacteriophages as well as by antagonistic microbes and competition for space in a suitable ecological niche. Therefore, diverse populations of organisms help to limit pathogen numbers [41]. Because of the ability of soils to
Figure 2
Exposure to attractive natural landscapes, which are underpinned by soils, has been shown to produce positive health benefits, and soils are an important consideration when properly planning recreational features such as hiking trails. These are examples of cultural services provided by soil. Photo by E.C. Brevik. www.sciencedirect.com
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regulate pathogens, well designed, properly maintained and functioning on-site sewage treatment systems are highly effective at reducing water-borne diseases in areas with low population densities [42]. Soil biota are also involved in decontaminating the environment from toxic waste by phytoremediation and microbial bioremediation [43,44], again highlighting the importance of soil biodiversity to human health. In fact, the use of soils to address groundwater contamination issues has been one of the fastest growing areas of soil science in recent years [45]. Finally, soil biodiversity is important for maintaining soil physical structure and preventing soil degradation. Fungal hyphae networks, together with microbial glues and slimes produced by OM degradation, bind primary inorganic particles into soil aggregates and plant roots stabilize loose soil [46]. This is important in soil conservation and also reduces dust and thus the spread of pathogens to humans and animals [2]. Links to the soil ES water purification and waste treatment and regulation of diseases can be seen in this example. Soils are intimately linked to the cycling of several greenhouse gases, including CO2 (Figure 3), CH4, and N2O, meaning these gases fall within the regulating services provided by soils. Human management of soils can either increase or decrease the levels of carbon and nitrogen based gases in the atmosphere [38], and the presence of these gases may cause a number of health
problems for humans [2]. Human management of soils can influence the balance between C and N sequestered in and the emissions of C and N containing gases from soils. The type of tillage used to manage agricultural fields, the number of machine passes (which influences soil organic matter decomposition rates and fuel consumption), crop rotations, use of cover crops, types of fertilizer used, types of organic residues applied and whether they are incorporated into the soil or left on the soil surface, and the length of the flooded period in rice paddies are all management decisions that influence the C and N balances in agricultural soils and represent direct interactions between soils and atmospheric greenhouse gas levels [38,47]. Here too the importance of soil biodiversity and the presence of varied microbial functional groups that are involved in nutrient cycling is highlighted [33]. The quality of food is also affected. A meta-analysis demonstrated that increased atmospheric CO2 decreases overall mineral concentrations and increases the ratio of carbohydrates to minerals in 130 varieties of plants, increasing the likelihood of hidden hunger and obesity [48]. Links to the ES climate regulation can be seen in this example.
Cultural services Cultural services refer to the non-material, and normally non-rival and non-consumptive outputs of ecosystems (biotic and abiotic) that affect the physical and mental
Figure 3
Soil is an important part of several cycles, including the carbon cycle. This diagram provides a simplified summary of the role soil plays in the carbon cycle, which is in turn important in regulating planetary temperatures. Soil plays an important role in human health through its influence on climate, a regulating service.
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states of people [12]. The MEA defined these as nonmaterial benefits people obtain from ecosystems through spiritual enrichment, cognitive development, reflection, recreation, and aesthetic experiences [11]. The horticultural community has conducted studies that demonstrate exposure to plants speeds the healing process for patients after surgery [49], walking through a garden helps restore mental clarity [50], and stress reduction and restoration from mental fatigue have been documented for people exposed to attractive landscapes [51,52] (Figure 2). Care farming, where commercial farms and agricultural landscapes are used to promote mental and physical health during the course of normal farming activity [53], has also been shown to improve mental, physical, and social health [53e55]. In each of these cases, soils are the medium within which the garden plants grow or agriculture is carried out. In this context, soils have an indirect benefit on human health. However, additional direct benefits have also been examined; for example, gardeners may respond positively to working with soil [56]. Soils are also important in recreation. The most direct link is probably gardening, where the gardener works with soil. Gardening has been shown to improve mental and physical health as well as encourage healthy eating through increased consumption of fresh fruits and vegetables [57,58]. While this is an indirect health link, Hanyu et al. [59] have documented exposure to healthy soils leading to a state of physiological and mental relaxation and reduced stress. Recreational activities such as hiking, camping, and biking also improve mental and physical health [60,61], and soils information is important in planning trails and campsites to maximize the recreational experience (Figure 2). The US National Cooperative Soil Survey has included information on the suitability of soils for a variety of recreational activities in their soil survey reports since the 1960s [62]. Therefore, soils contribute both directly and indirectly to the promotion of human health through cultural services.
Concluding statements It is important to note that the issues discussed in this paper are examples, not comprehensive discussions of the ways that soil ES influence human health. The space available here is too short for a comprehensive discussion. However, this paper does point out clear examples of ways that human health is linked to soil ES. Furthermore, it demonstrates that taking an ES approach when considering soils and human health has the potential to identify areas that need further investigation, such as the influence of soils on human health through the provisioning of building materials, fiber, and fuel. Lastly, the importance of avoiding or correcting soil degradation to provide the healthy soils necessary to maximize soil ES that support human health cannot be overlooked. To this point the soils and human health literature has not focused on connections between soil ES and human health. An increased focus on this area in the future would be beneficial. www.sciencedirect.com
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Conflict of interest statement Nothing declared.
Acknowledgements E. Brevik and J. Steffan were partially supported by the National Science Foundation under Grant Number IIA-1355466 during this project.
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