Biodiversity loss and the ecology of infectious disease
Authors: Richard S Ostfeld
Journal: The Lancet Planetary Health (2017)

As a new discipline, the field of planetary health could follow one of two obvious pathways. In the first, practitioners of planetary health would develop a catalogue of the myriad ways in which human health is affected by anthropogenic changes to the environment. Although such an exercise might be valuable, it would not be novel, and the information by itself might not lead to solutions to the critical problems being documented. In the second pathway, planetary health practitioners would use the many adverse health consequences of anthropogenic environmental change as grounds to advocate for better environmental protections. Although there is no doubt that advocacy is necessary to prevent ever more rapid degradation of environmental health, this pathway would de-emphasise the scientific mission of planetary health and emphasise the political one. I argue that there is a third path. Planetary health could document the many cases in which human health and environmental health are simultaneously improved by the same policy or management actions. A thorough exploration of these win–win situations, with careful analysis of the mechanisms that underlie co-benefits to environmental and human health, could uncover key principles and inform new applications, while providing concrete options for policy and management. Environmental health and human health are both multidimensional concepts. Identification of principles underlying win–win situations requires identification of specific, measurable components of both environmental and human health. In the example that follows, I specify species diversity (a key component of biodiversity) as a focal metric of environmental health and risk of exposure to zoonotic diseases as a focal metric of human health. Burgeoning research has shown that high biodiversity frequently reduces rates of pathogen transmission and lowers disease risk for human beings, wildlife, livestock, and plants.1Keesing F Belden LK Daszak P et al.Impacts of biodiversity on the emergence and transmission of infectious diseases.Nature. 2010; 468: 647-652Crossref PubMed Scopus (1143) Google Scholar, 2Ostfeld RS Keesing F Effects of host diversity on infectious disease.Annu Rev Ecol Evol Syst. 2012; 43: 157-182Crossref Scopus (45) Google Scholar, 3Ostfeld RS, Keesing F. Is biodiversity bad for your health? Ecosphere (in press).Google Scholar, 4Civitello DJ Cohen J Fatima H et al.Biodiversity inhibits parasites: broad evidence for the dilution effect.Proc Natl Acad Sci USA. 2015; 112: 8667-8671Crossref PubMed Scopus (370) Google Scholar, 5Huang ZYX Van Langevelde F Estrada-Peña A Suzan G De Boer WF The diversity-disease relationship: evidence for and criticisms of the dilution effect.Parasitology. 2016; 143: 1075-1086Crossref PubMed Scopus (43) Google Scholar The widespread inhibitory effect of high biodiversity on pathogen transmission arises from a set of mechanisms that are actively being researched. First, most pathogens seem to be host generalists, in the sense that they encounter and potentially infect more than one species of host. Second, these host species differ substantially in their invasibility, susceptibility to infection, and potential to transmit infection to other hosts. Third, in many cases, the hosts most likely to acquire and transmit infection (the so-called reservoir hosts) are species that are abundant, widespread, and resilient to anthropogenic perturbations. Consequently, these reservoir species tend to persist when diversity is reduced, increasing in abundance relative to species more sensitive to disturbance. Consequently, species living in ecological communities with high diversity tend to dilute the effect of the reservoir species and reduce disease risk.6Keesing F Holt RD Ostfeld RS Effects of species diversity on disease risk.Ecology Letters. 2006; 9: 485-498Crossref PubMed Scopus (1015) Google Scholar This "dilution effect"6Keesing F Holt RD Ostfeld RS Effects of species diversity on disease risk.Ecology Letters. 2006; 9: 485-498Crossref PubMed Scopus (1015) Google Scholar, 7Ostfeld RS Keesing F The function of biodiversity in the ecology of vector-borne zoonotic diseases.Can J Zool. 2000; 78: 2061-2078Crossref Google Scholar of high diversity has been best studied in plant and wildlife diseases but is also known to be widespread in human pathogens.2Ostfeld RS Keesing F Effects of host diversity on infectious disease.Annu Rev Ecol Evol Syst. 2012; 43: 157-182Crossref Scopus (45) Google Scholar, 8Civitello DJ Cohen J Fatima H et al.Reply to Salkeld et al.: diversity-disease patterns are robust to study design, selection criteria, and publication bias.Proc Natl Acad Sci USA. 2015; 112: E6262Crossref PubMed Scopus (8) Google Scholar Its operation can be understood from the following observations. First, most human infectious diseases are zoonotic in origin.9Woolhouse MEJ Gowtage-Sequeria S Host range and emerging and reemerging pathogens.Emerg Infect Dis. 2005; 11: 1842-1847Crossref PubMed Scopus (918) Google Scholar These zoonotic pathogens are capable of infecting multiple species of host. Second, although zoonotic pathogens can originate in many different species of vertebrates, certain mammalian orders are over-represented as pathogen sources. Rodents, in particular, carry more zoonotic pathogens than do any other mammalian order, and far more rodent species host zoonotic pathogens than do other orders.10Han BA Kramer AM Drake JM Global patterns of zoonotic disease in mammals.Trends Parasitol. 2016; 32: 565-577Summary Full Text Full Text PDF PubMed Scopus (215) Google Scholar Even within the rodents, the species with fast life history traits (early maturity, large litters, and short longevity) are more likely than species with slower life histories to be reservoirs for zoonotic pathogens.11Han BA Schmidt JP Bowden SE Drake JM Rodent reservoirs of future zoonotic diseases.Proc Natl Acad Sci USA. 2015; 112: 7039-7044Crossref PubMed Scopus (287) Google Scholar Third, fast life histories are typically associated with commonness and resilience to disturbance,12Stearns SC The evolution of life histories. Oxford University Press, London1992Google Scholar suggesting that competent reservoir species will often predominate in low-diversity communities. The propensity for species of plants and animals with fast life history traits to be among the best reservoirs for multi-host pathogens is under active investigation. One possible underlying mechanism could be a tendency for species with fast life histories to have lower resistance or higher tolerance to infection, resulting from trade-offs between reproduction and self-defence.13Ostfeld RS Levi T Jolles AE Martin LB Hosseini PR Keesing F Life history and demographic drivers of reservoir competence for three tick-borne zoonotic pathogens.PLoS One. 2014; 9: e107387Crossref PubMed Scopus (83) Google Scholar Another possible mechanism could be a tendency for multi-host pathogens to specialise on host species that they encounter most frequently, which might be hosts with high average population density.7Ostfeld RS Keesing F The function of biodiversity in the ecology of vector-borne zoonotic diseases.Can J Zool. 2000; 78: 2061-2078Crossref Google Scholar Irrespective of the mechanisms, whenever pathogen transmission or disease risk is lower in high-diversity communities, policies that prevent the loss of biodiversity will simultaneously promote environmental protection and health protection. How common are win–win situations like this, in which a single policy or management option might improve both environmental protection and human health? Are there specific features shared in common by these situations? When trade-offs between environmental and human health prevail, can policy be adjusted to reduce the costs to the environment or to people? To what degree does the characterisation of a policy as win–win versus trade-off depend on the specific environmental health or human health outcome being considered? How frequently is the identification of win–win situations limited by data, and how can data limitations be breached? Planetary health is uniquely poised to address these and related questions, the answers to which will undoubtedly improve both science and health. The urgency of this enterprise grows as assaults on the environment accelerate. I declare no competing interests. I acknowledge helpful input from Felicia Keesing.