Soil biodiversity and human health

Abstract

Soil biodiversity is increasingly recognized as providing benefits to human health because it can suppress disease-causing soil organisms and provide clean air, water and food. Poor land-management practices and environmental change are, however, affecting belowground communities globally, and the resulting declines in soil biodiversity reduce and impair these benefits. Importantly, current research indicates that soil biodiversity can be maintained and partially restored if managed sustainably. Promoting the ecological complexity and robustness of soil biodiversity through improved management practices represents an underutilized resource with the ability to improve human health.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Flow diagram illustrating the link between soil biodiversity and human health.
Figure 2: A conceptual framework illustrating how decisions on land use and management are linked to human health through the effect on soil biodiversity.

References

  1. 1

    Bardgett, R. D. & van der Putten, W. H. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511 (2014)

    CAS  Article  ADS  PubMed  PubMed Central  Google Scholar 

  2. 2

    Fisher, F. S., Bultman, M. W., Johnson, S. M., Pappagianis, D. & Zaborsky, E. Coccidioides niches and habitat parameters in the southwestern United States: a matter of scale. Ann. NY Acad. Sci. 1111, 47–72 (2007)

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  3. 3

    Wall, D. H. et al. Soil Ecology and Ecosystem Services (Oxford Univ. Press, 2012)

  4. 4

    Wall, D. H. & Six, J. Give soils their due. Science 347, 695 (2015)

    CAS  Article  ADS  PubMed  PubMed Central  Google Scholar 

  5. 5

    Haddad, N. M. et al. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci. Adv. 1, e1500052 (2015)

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  6. 6

    Tsiafouli, M. A. et al. Intensive agriculture reduces soil biodiversity across Europe. Glob. Change Biol. 21, 973–985 (2015).This study, encompassing four agricultural regions across Europe, showed that increasing land-use intensity reduced soil foodweb diversity, functional diversity and taxonomic diversity.

    Article  ADS  Google Scholar 

  7. 7

    Garrison, V. H. et al. African and Asian dust: from desert soils to coral reefs. Bioscience 53, 469–480 (2003)

    Article  Google Scholar 

  8. 8

    Park, J. W. et al. Effects of ambient particulate matter on peak expiratory flow rates and respiratory symptoms of asthmatics during Asian dust periods in Korea. Respirology 10, 470–476 (2005)

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9

    Quinton, J. N., Govers, G., Van Oost, K. & Bardgett, R. D. The impact of agricultural soil erosion on biogeochemical cycling. Nature Geosci. 3, 311–314 (2010)

    CAS  Article  ADS  Google Scholar 

  10. 10

    Schenker, M. Exposures and health effects from inorganic agricultural dusts. Environ. Health Perspect. 108, 661–664 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11

    Dominati, E., Patterson, M. & Mackay, A. A framework for classifying and quantifying the natural capital and ecosystem services of soils. Ecol. Econ. 69, 1858–1868 (2010)

    Article  Google Scholar 

  12. 12

    Thiele-Bruhn, S., Bloem, J., de Vries, F. T., Kalbitz, K. & Wagg, C. Linking soil biodiversity and agricultural soil management. Curr. Opin. Environ. Sustainability 4, 523–528 (2012)

    Article  Google Scholar 

  13. 13

    Nielsen, U. N., Wall, D. H. & Six, J. Soil biodiversity and the environment. Annu. Rev. Environ. Resour. 40, 63–90 (2015)

    Article  Google Scholar 

  14. 14

    World Health Organization and Secretariat of the Convention on Biological Diversity. Connecting Global Priorities: Biodiversity and Human Health. A State of Knowledge Review https://www.cbd.int/health/SOK-biodiversity-en.pdf (WHO, 2015)

  15. 15

    Brevik, E. C. & Burgess, L. C. The 2012 fungal meningitis outbreak in the United States: connections between soils and human health. Soil Horizons 54, 1–4 (2013)

    Article  Google Scholar 

  16. 16

    Oliver, M. A. & Gregory, P. J. Soil, food security and human health: a review. Eur. J. Soil Sci. 66, 257–276 (2015)

    Article  Google Scholar 

  17. 17

    Ling, L. L. et al. A new antibiotic kills pathogens without detectable resistance. Nature 517, 455–459 (2015)

    CAS  Article  ADS  Google Scholar 

  18. 18

    Ferris, H. & Tuomisto, H. Unearthing the role of biological diversity in soil health. Soil Biol. Biochem. 85, 101–109 (2015)

    CAS  Article  Google Scholar 

  19. 19

    Brevik, E. C. & Burgess, L. C. Soils and Human Health (CRC Press, 2012)

  20. 20

    Bultman, M. W., Fisher, F. S. & Pappagianis, D. in Essentials of Medical Geology (ed. O. Selinus ) Ch. 20 (Springer, 2013)

  21. 21

    Pepper, I. L., Gerba, C. P., Newby, D. T. & Rice, C. W. Soil: a public health threat or savior? Crit. Rev. Environ. Sci. Technol. 39, 416–432 (2009)

    Article  Google Scholar 

  22. 22

    Brevik, E. C. & Sauer, T. J. The past, present, and future of soils and human health studies. Soil 1, 35–46 (2015)

    Article  Google Scholar 

  23. 23

    Myers, S. S. & Patz, J. A. Emerging threats to human health from global environmental change. Annu. Rev. Environ. Resour. 34, 223–252 (2009)

    Article  Google Scholar 

  24. 24

    Berg, G., Eberl, L. & Hartmann, A. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ. Microbiol. 7, 1673–1685 (2005)

    CAS  Article  Google Scholar 

  25. 25

    Ganz, H. H. et al. Interactions between Bacillus anthracis and plants may promote anthrax transmission. PLoS Negl. Trop. Dis. 8, http://dx.doi.org/10.1371/journal.pntd.0002903 (2014)

  26. 26

    Smith, K. L. et al. Bacillus anthracis diversity in Kruger National Park. J. Clin. Microbiol. 38, 3780–3784 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27

    Schär, F. et al. Strongyloides stercoralis: global distribution and risk factors. PLoS Negl. Trop. Dis. 7, http://dx.doi.org/10.1371/journal.pntd.0002288 (2013)

  28. 28

    Khieu, V. et al. High prevalence and spatial distribution of Strongyloides stercoralis in rural Cambodia. PLoS Negl. Trop. Dis. 8, http://dx.doi.org/10.1371/journal.pntd.0002854 (2014)

  29. 29

    de Silva, N. R. et al. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol. 19, 547–551 (2003)

    Article  Google Scholar 

  30. 30

    Kay, A. B. Overview of “Allergy and allergic diseases: with a view to the future”. Br. Med. Bull. 56, 843–864 (2000)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. 31

    Matricardi, P. M. & Bonini, S. High microbial turnover rate preventing atopy: a solution to inconsistencies impinging on the hygiene hypothesis? Clin. Exp. Allergy 30, 1506–1510 (2000)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. 32

    Rook, G. A. W. 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: Darwinian medicine and the 'hygiene' or 'old friends' hypothesis. Clin. Exp. Immunol. 160, 70–79 (2010)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33

    Hanski, I. et al. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc. Natl Acad. Sci. USA 109, 8334–8339 (2012). This study provides evidence that people living near environmentally diverse areas had less propensity for allergies because of a greater diversity of commensal bacteria on their skin, most of which are also found in soil and vegetation.

    CAS  Article  ADS  PubMed  PubMed Central  Google Scholar 

  34. 34

    Haahtela, T. et al. The Finnish Allergy Programme 2008–2018—scientific rationale and practical implementation. Asia Pacific Allergy 2, 275–279 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  35. 35

    Ruokolainen, L. et al. Green areas around homes reduce atopic sensitization in children. Allergy 70, 195–202 (2015)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36

    Prichard, R. in Antimicrobial Drug Resistance (ed. Mayers, D. L. ) 621–628 (Springer, 2009)

  37. 37

    Corbett, C. J. et al. The effectiveness of faecal removal methods of pasture management to control the cyathostomin burden of donkeys. Parasites Vectors 7, 48 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  38. 38

    Epstein, L. Fifty years since Silent Spring. Annu. Rev. Phytopathol. 52, 377–402 (2014)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. 39

    Campos-Herrera, R., El-Borai, F. E. & Duncan, L. W. in Nematode Pathogenesis of Insects and Other Pests (ed. Campos-Herrera, R. ) (Springer, 2015)

  40. 40

    Charles, L. et al. Phylogenetic analysis of Pasteuria penetrans by use of multiple genetic loci. J. Bacteriol. 187, 5700–5708 (2005)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. 41

    Gray, N. F. Ecology of nematophagous fungi: Panagrellus redivivus as the target organism. Plant Soil 73, 293–297 (1983)

    Article  Google Scholar 

  42. 42

    Stirling, G. R. in Biological Control of Plant-Parasitic Nematodes: Building Coherence Between Microbial Ecology and Molecular Mechanisms (eds Davies, K. G. & Spiegel, Y. ) 1–38 (Springer, 2011)

  43. 43

    Stirling, G. R. Biological Control of Plant-Parasitic Nematodes: Soil Ecosystem Management Sustainable Agriculture 2nd edn (CABI, 2014)

  44. 44

    Costa, S. R., Kerry, B. R., Bardgett, R. D. & Davies, K. G. Interactions between nematodes and their microbial enemies in coastal sand dunes. Oecologia 170, 1053–1066 (2012)

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  45. 45

    Ferris, H. et al. Diversity and complexity complement apparent competition: nematode assemblages in banana plantations. Acta Oecol. 40, 11–18 (2012)

    Article  ADS  Google Scholar 

  46. 46

    Sánchez-Moreno, S. & Ferris, H. Suppressive service of the soil food web: effects of environmental management. Agric. Ecosyst. Environ. 119, 75–87 (2007). This study showed that the prevalence of predator and omnivorous nematodes, which suppressed plant parasitic nematodes, was higher in soils with more complex foodwebs.

    Article  Google Scholar 

  47. 47

    Penton, C. R. et al. Fungal community structure in disease suppressive soils assessed by 28S LSU gene sequencing. PLoS ONE 9, http://dx.doi.org/10.1371/journal.pone.0093893 (2014)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  48. 48

    Weller, D. M., Raaijmakers, J. M., Gardener, B. B. M. & Thomashow, L. S. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40, 309–348 (2002)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. 49

    Johnson, P. T. J. et al. Species diversity reduces parasite infection through cross-generational effects on host abundance. Ecology 93, 56–64 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  50. 50

    Johnson, P. T. J., Preston, D. L., Hoverman, J. T. & Richgels, K. L. D. Biodiversity decreases disease through predictable changes in host community competence. Nature 494, 230–233 (2013). This laboratory and field study showed that a richer host diversity reduced transmission of a parasite (the trematode Ribeiroia ondatrae ) and reduced amphibian disease.

    CAS  Article  ADS  Google Scholar 

  51. 51

    Keesing, F., Holt, R. D. & Ostfeld, R. S. Effects of species diversity on disease risk. Ecol. Lett. 9, 485–498 (2006)

    CAS  Article  Google Scholar 

  52. 52

    Searle, C. L., Biga, L. M., Spatafora, J. W. & Blaustein, A. R. A dilution effect in the emerging amphibian pathogen Batrachochytrium dendrobatidis. Proc. Natl Acad. Sci. USA 108, 16322–16326 (2011)

    CAS  Article  ADS  Google Scholar 

  53. 53

    Suzán, G. et al. Experimental evidence for reduced rodent diversity causing increased hantavirus prevalence. PLoS ONE 4, http://dx.doi.org/10.1371/journal.pone.0005461 (2009)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  54. 54

    van Elsas, J. D. et al. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc. Natl Acad. Sci. USA 109, 1159–1164 (2012). Experimental results showed that in soils with greater microbial diversity invading bacteria have a lower survival rate.

    CAS  Article  ADS  Google Scholar 

  55. 55

    Andersen, D. C. Belowground herbivory in natural communities—a review emphasizing fossorial animals. Q. Rev. Biol. 62, 261–286 (1987)

    Article  Google Scholar 

  56. 56

    Gehring, C. A., Wolf, J. E. & Theimer, T. C. Terrestrial vertebrates promote arbuscular mycorrhizal fungal diversity and inoculum potential in a rain forest soil. Ecol. Lett. 5, 540–548 (2002)

    Article  Google Scholar 

  57. 57

    Bates, S. T. et al. Global biogeography of highly diverse protistan communities in soil. ISME J. 7, 652–659 (2013)

    CAS  Article  Google Scholar 

  58. 58

    Wu, T., Ayres, E., Bardgett, R. D., Wall, D. H. & Garey, J. R. Molecular study of worldwide distribution and diversity of soil animals. Proc. Natl Acad. Sci. USA 108, 17720–17725 (2011)

    CAS  Article  ADS  Google Scholar 

  59. 59

    Ramirez, K. S. et al. Biogeographic patterns in below-ground diversity in New York City's Central Park are similar to those observed globally. Proc. R. Soc. B 281, http://dx.doi.org/10.1098/rspb.2014.1988 (2014)

  60. 60

    Lauber, C. L., Ramirez, K. S., Aanderud, Z., Lennon, J. & Fierer, N. Temporal variability in soil microbial communities across land-use types. ISME J. 7, 1641–1650https://doi.org/10.1038/ismej.2013.50 (2013)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. 61

    Tedersoo, L. et al. Global diversity and geography of soil fungi. Science 346, http://dx.doi.org/10.1126/science.1256688 (2014). This analysis indicates that the distribution and species richness of fungi is mostly determined by climate and not related to plant diversity on a global scale, except for root-related ectomycorrizal fungi; biogeographical comparisons of continents indicate efficient dispersal mechanisms for fungi compared to larger organisms.

  62. 62

    van Groenigen, J. W. et al. Earthworms increase plant production: a meta-analysis. Sci. Rep. 4, http://dx.doi.org/10.1038/srep06365 (2014)

  63. 63

    Evans, T. A., Dawes, T. Z., Ward, P. R. & Lo, N. Ants and termites increase crop yield in a dry climate. Nature Commun. 2, http://dx.doi.org/10.1038/ncomms1257 (2011)

  64. 64

    Bender, S. F. & van der Heijden, M. G. A. Soil biota enhance agricultural sustainability by improving crop yield, nutrient uptake and reducing nitrogen leaching losses. J. Appl. Ecol. 52, 228–239 (2015)

    CAS  Article  Google Scholar 

  65. 65

    de Vries, F. T. et al. Soil food web properties explain ecosystem services across European land use systems. Proc. Natl Acad. Sci. USA 110, 14296–14301 (2013)

    CAS  Article  ADS  Google Scholar 

  66. 66

    de Vries, F. T. et al. Land use alters the resistance and resilience of soil food webs to drought. Nature Clim. Change 2, 276–280 (2012). This study compared nitrogen retention in extensive versus intensive grasslands and showed that species-rich extensively managed grasslands had greater soil nitrogen retention due to a higher fungal:bacterial abundance ratio compared to intensively managed grasslands.

    Article  ADS  Google Scholar 

  67. 67

    Wall, D. H., Bardgett, R. D. & Kelly, E. F. Biodiversity in the dark. Nature Geosci. 3, 297–298 (2010)

    CAS  Article  ADS  Google Scholar 

  68. 68

    Rillig, M. C. & Mummey, D. L. Mycorrhizas and soil structure. New Phytol. 171, 41–53 (2006)

    CAS  Article  Google Scholar 

  69. 69

    Schulin, R., Khoshgoftarmanesh, A., Afyuni, M., Nowack, B. & Frossard, E. in Development and Uses of Biofortified Agricultural Products (eds Banuelos, G. S. & Lin, Z.-Q. ) Ch. 6 (CRC Press, 2008)

  70. 70

    Rodriguez, R. J. et al. Stress tolerance in plants via habitat-adapted symbiosis. ISME J. 2, 404–416 (2008)

    Article  PubMed  PubMed Central  Google Scholar 

  71. 71

    Brown, J. K. M. & Hovmøller, M. S. Epidemiology—aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297, 537–541 (2002)

    CAS  Article  ADS  PubMed  PubMed Central  Google Scholar 

  72. 72

    Nkem, J. N. et al. Wind dispersal of soil invertebrates in the McMurdo Dry Valleys, Antarctica. Polar Biol. 29, 346–352 (2006)

    Article  Google Scholar 

  73. 73

    Madden, N. M., Southard, R. J. & Mitchell, J. P. Conservation tillage reduces PM10 emissions in dairy forage rotations. Atmos. Environ. 42, 3795–3808 (2008)

    CAS  Article  ADS  Google Scholar 

  74. 74

    Sprigg, W. A. et al. Regional dust storm modeling for health services: the case of valley fever. Aeolian Res. 14, 53–73 (2014)

    Article  ADS  Google Scholar 

  75. 75

    Nguyen, C. et al. Recent advances in our understanding of the environmental, epidemiological, immunological, and clinical dimensions of coccidioidomycosis. Clin. Microbiol. Rev. 26, 505–525 (2013)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  76. 76

    Tabor, J. A., O'Rourke, M. K., Lebowitz, M. D. & Harris, R. B. Landscape-epidemiological study design to investigate an environmentally based disease. J. Expo. Sci. Environ. Epidemiol. 21, 197–211 (2011)

    Article  PubMed  PubMed Central  Google Scholar 

  77. 77

    Frey, S. D., Elliott, E. T. & Paustian, K. Bacterial and fungal abundance and biomass in conventional and no-tillage agroecosystems along two climatic gradients. Soil Biol. Biochem. 31, 573–585 (1999)

    CAS  Article  Google Scholar 

  78. 78

    Six, J., Frey, S. D., Thiet, R. K. & Batten, K. M. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci. Soc. Am. J. 70, 555–569 (2006)

    CAS  Article  ADS  Google Scholar 

  79. 79

    Anderson, J. O., Thundiyil, J. G. & Stolbach, A. Clearing the air: a review of the effects of particulate matter air pollution on human health. J. Med. Toxicol. 8, 166–175 (2012). This review provides an analysis of the complexity of particulate matter air pollution and its effects on human health.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  80. 80

    Nordstrom, K. F. & Hotta, S. Wind erosion from cropland solutions in the USA: a review of problems, and prospects. Geoderma 121, 157–167 (2004)

    Article  ADS  Google Scholar 

  81. 81

    Alavanja, M. C. R., Ross, M. K. & Bonner, M. R. Increased cancer burden among pesticide applicators and others due to pesticide exposure. CA Cancer J. Clin. 63, 120–142 (2013)

    Article  Google Scholar 

  82. 82

    Frankenberger, W. T. & Arshad, M. Bioremediation of selenium-contaminated sediments and water. Biofactors 14, 241–254 (2001)

    CAS  Article  Google Scholar 

  83. 83

    Abraham, J. & Silambarasan, S. Biodegradation of chlorpyrifos and its hydrolyzing metabolite 3,5,6-trichloro-2-pyridinol by Sphingobacterium sp JAS3. Process Biochem. 48, 1559–1564 (2013)

    CAS  Article  Google Scholar 

  84. 84

    Rayu, S., Karpouzas, D. G. & Singh, B. K. Emerging technologies in bioremediation: constraints and opportunities. Biodegradation 23, 917–926 (2012)

    CAS  Article  Google Scholar 

  85. 85

    Bailey, R. T., Romero, E. C. & Gates, T. K. Assessing best management practices for remediation of selenium loading in groundwater to streams in an irrigated region. J. Hydrol. 521, 341–359 (2015)

    CAS  Article  ADS  Google Scholar 

  86. 86

    Tiemann, L., Grandy, A., Atkinson, E., Marin-Spiotta, E. & McDaniel, M. Crop rotational diversity enhances belowground communities and functions in an agrosystem. Ecol. Lett. 18, 761–771 (2015)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  87. 87

    Chauvat, M., Titsch, D., Zaytsev, A. S. & Wolters, V. Changes in soil faunal assemblages during conversion from pure to mixed forest stands. For. Ecol. Manage. 262, 317–324 (2011)

    Article  Google Scholar 

  88. 88

    Cary, S. C. & Fierer, N. The importance of sample archiving in microbial ecology. Nature Rev. Microbiol. 12, 789–790 (2014)

    CAS  Google Scholar 

  89. 89

    Jeffery, S. & van der Putten, W. H. Soil-Borne Human Diseases 1–56, http://dx.doi.org/10.2788/37199 (Joint Research Centre Scientific and Technical Reports, European Commission, 2011)

  90. 90

    United Nations Sustainable Development Goals. Open Working Group Proposal for Sustainable Development Goals, https://sustainabledevelopment.un.org/focussdgs.html (UN, 2014)

Download references

Acknowledgements

We appreciate the encouragement of J. Lehmann to write this article, and acknowledge the comments of B. Adams, L. Duncan, A. Franco, T. Fraser, M. Knox, K. Pintauro, A. Shaw, A. Weller and S. Vandewoude. D.H.W. acknowledges the Winslow Foundation.

Author information

Affiliations

Authors

Contributions

D.H.W., J.S. and U.N.N. contributed equally to the planning and writing of the manuscript.

Corresponding author

Correspondence to Diana H. Wall.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wall, D., Nielsen, U. & Six, J. Soil biodiversity and human health. Nature 528, 69–76 (2015). https://doi.org/10.1038/nature15744

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing