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Marilyn Jordan: Is Biodiversity Loss Making Us Sick?

Marilyn Jordan, Senior Conservation Scientist 1/14/2013

parrchristyFlickr via Creative Commons
Biodiversity is rapidly declining, we know this. But so what? Unless you’re a conservationist, ecologist or environmental scientist, biodiversity is an abstract concept with little relevance to people’s everyday lives and health. Until now. Earlier this year, a groundbreaking study out of Finland became the first to provide evidence of a link between biodiversity loss and human inflammatory diseases (Hanski et al. 2012). The researchers’ “biodiversity hypothesis” — the idea that environmental biodiversity is linked to both microbial diversity and human health — has far-reaching implications for biodiversity protection and for improving public health. Could it even transform the conservation movement? We’ll get to that. But first, some background.
A Version of “Eating Dirt”
Perhaps you have heard of the “hygiene hypothesis,” colloquially known as “let them eat dirt.” Essentially, the hypothesis says that humans developed a dependence on a variety of commensal microbes with which we co-evolved (Rook 2010). Exposure to these microbial “old friends” remains essential for training the developing immune system of babies and toddlers to distinguish between dangerous pathogens and harmless microbes, and is still important in adulthood (Rook 2010).
According to the hygiene hypothesis, the increasing incidence of allergies (asthma, hay fever, atopic eczema) and autoimmune diseases (e.g. type 1 diabetes, inflammatory bowel disease, multiple sclerosis, depression) over the last few decades is largely due to limited exposure to microorganisms (bacteria, fungi, viruses and possibly protozoans). Antibiotic use, exposure to antibacterial soaps, high socioeconomic status, small family size, early birth order and more all tend to reduce exposure to indigenous microbiota
and contribute to allergic diseases. So the absence of good microbial species can make us sick.
The focus of the hygiene hypothesis was on microbial exposure only in the home, food, drinking water and from animals — until Finnish researchers von Hertzen, Hanski and Haahtela expanded the hygiene/microbial deprivation hypothesis to a biodiversity hypothesis (von Hertzen et al. 2012). They proposed that environmental biodiversity is linked to both microbial diversity and human health. Their hypothesis links two seemingly unrelated trends: Rapid growth of urban populations (UNDP 2009) which have limited exposure to biodiversity, and a skyrocketing increase in the incidence of allergies and other chronic inflammatory diseases in urban areas (Fig. 1). Their data were published this spring and will likely lead to an explosion of new research (Hanski et al.2012). If their findings are replicated by others it could lead to major changes in thinking about biodiversity and disease.
sc jan 13 jordan biodiversity fig 1.jpg
Figure 1: Two global megatrends in biodiversity and public health. (A) Declining biodiversity since 1970 as measured by three indices. LPI, Living Planet Index; WBI, World Bird Index; WPSI, Waterbird Population Status Index (Butchart et al. 2010). (B) Increasing trends in the prevalence of inflammatory diseases. Asthma and allergic rhinitis among military conscripts from 1966 to 2003 (Latvala et al. 2005) are shown as an example.
Reprinted by permission from Macmillan Publishers Ltd: von Hertzen L, Hanski I, Haahtela T. Natural Immunity. EMBO Reports 12:1089–1093, 2011.
The Negative Correlation of Wild Native Flowering Plants and Atopy
What Hanski and colleagues did was to relate the atopy (allergic disposition as measured by the level of IgE antibodies) of adolescents in eastern Finland to microbial diversity on their skin, and to the environmental biodiversity of their yards and surrounding land use types. Atopic individuals had significantly lower generic diversity of gammaproteobacteria on their skin and were more likely to live in built areas or near large water bodies rather than in forested or agricultural lands. (Gammaproteobacteria are a diverse class of bacteria found in dust, soil, ambient air and on pollen grains but are particularly dominant in vegetation.)
Interestingly, they also found that species richness of just one group of plants — wild native flowering plants — was significantly correlated with atopy. Adolescents who lived in homes with a greater diversity of native flowering plants in their yards had a lower incidence of atopy. No association between plant diversity and gammaproteobacteria was found, though Hanski told me such a link may be found in future studies.
These observations were supported by in vitro measurements of IL-10, a key antiinflammatory signaling molecule released by immune system cells. IL-10 in blood cells was positively correlated with the abundance of the gammaproteobacterial genus Acinetobacter in healthy individuals. Hanski thinks that low diversity of gammaproteobacteria is much more likely to be a cause of allergic disease rather than the reverse, based on previous immunological and experimental studies.
Reasons and mechanisms for the link to flowering plants are unclear (see diagram 1),for bacterial diversity on plants has not yet been studied. A diverse plant community may support a diverse microbial community, which directly benefits people. However the amount and diversity of pollen may also play a role or high diversity of flowering plants may simply indicate a more natural state of residents’ yards. In the Finnish study area, many yards were not carefully managed so vegetation in parts of the yards is similar to natural areas, Hanski explained to me.
sc jan 13 jordan biodiversity diagram 1.jpg
Diagram 1: Adapted by M. Jordan from Hanski et al. 2012. Hanski et al. 2012. Diagram 1 legend: Associations among environmental diversity, skin microbiota and atopy. Solid arrows indicate P<0.015 to <0.0009; dashed arrow P=0.059. IL-10 is a key anti-inflammatory cytokine (immune system signaling molecule).
Hanski thinks that the general effects they observed are probably universal but details may differ in other biogeographic regions. Plant diversity in Finland is low, and the largest town in the study area was Joensuu, population 73,000. Similar research is clearly needed from other regions that differ in population sizes, environmental conditions, plant diversity, and factors known to be related to health (diet, pollution levels, chemical exposure, etc.) to test and extend their findings.
One challenge to replicating their research is locating appropriate human populations. Most Finnish study subjects lived where they were born and grew up, which is important since it is exposure to microbes and allergens early in life that is most protective. Hanski and his colleagues plan to study populations in Russia, on the other side of the border with Finland. People in eastern Finland and adjacent Russia are genetically similar, but the Russians are less affluent and have much lower rates of asthma, allergies and type 1 diabetes.

Results of the Finnish research raise many questions ripe for research, including:
• Will the findings of Hanski et al. be replicated in other biogeographic regions and cultures, and in large cities, towns and suburbs?
• If so, by what mechanisms is plant diversity linked to reduced human immune diseases? Is it through direct causality or indirectly through other factors shared in common?
• Do novel no-analogue ecosystems dominated by relatively few species of spontaneous and cultivated nonnative plants support fewer genera and species of microbes beneficial to people compared with more diverse and/or mostly native plant assemblages?
• How much nature in cities is enough for all aspects of human physical and mental health, and how should it be distributed? Close proximity to green space is important, but do all urban residents utilize these areas?
Inevitably there will be a search for easy substitutes for biodiversity. Could we solve the inflammatory disease problem by sprinkling good bacteria on our potted houseplants, swallowing probiotics, and kissing the dog? Even if immune-stimulating treatments are developed, we will still need natural green places near where we live for many reasons, including relieving stress, encouraging physical activity, making social contacts and improving air quality, all of which contribute to physical and mental health (Maas et al. 2009).
Protection from chronic inflammatory disorders may turn out to be another reason for preserving not just green places, but the biodiversity of all life forms on earth. Yet more than 80% of people in the U.S. live in urban areas and the rest of the world is quickly catching up (UNDP 2009). As cities grow there is less room for natural environments. Von Hertzen and Hanski (2011) fear dire consequences for public health (and economies) if large numbers of people develop immune disorders requiring long lasting medical treatment as a result of microbe-poor environments.
What should we in The Nature Conservancy do? At first I think we should pay attention to this emerging area of research and investigate opportunities to be involved in interdisciplinary efforts to replicate Hanski’s findings. Do we have databases that
could be of use for biodiversity/health researchers? Could some of our preserves be good study areas? The Urban Homogenization Project would be a good place to start.
If the findings of Hanski et al. are found to be generally applicable in many biogeographic areas, it could transform conservation efforts. Biodiversity and conserving nature would be much more relevant to people, especially in urban areas. At this point, TNC should become actively involved. We should incorporate and monitor microbial diversity in our work at key sites (e.g. Parker 2010), and explore the possible benefits to immune system health provided by our urban and suburban preserves.
Our new strategy of establishing urban conservation initiatives could include efforts to link biodiversity of green spaces with all aspects of human health, not just immunological health. Since socioeconomically disadvantaged urban populations typically have the least exposure to natural areas and have poorer health, we should consider collaborative efforts with advocates for public health and environmental justice. 
As Stevens pointed out in Science Chronicles (2011), urban dwellers know “… there’s something they want that they can’t get from soccer fields and manicured city parks.” Who knew reduced incidence of allergic diseases might be one of those previously unidentified benefits?
Hanski, I. et al. 2012. Environmental biodiversity, human microbiota, and allergy are interrelated. Proceedings of the National Academy of Sciences, USA 109(21)8334-8339.
Maas, J. et al. 2009. Morbidity is related to a green living environment. Journal of Epidemiology & Community Health. 63:967–973.
Parker, S. 2010. Buried treasure: soil biodiversity and conservation. Biodiversity and Conservation. 19(13):3743-3756. Interview in Science Chronicles, January 2011.
Rook, GAW. 2010. Darwinian medicine and the ‘hygiene’ or ‘old friends’ hypothesis. 99th Dahlem Conference. Clinical and Experimental Immunology 160:70–79.
Stevens, P. 2011. Cities and conservation: why the rules are different in cities. The Nature Conservancy’s Science Chronicles, February 2011:25-27.
UNPD.  2009. World Urbanization Prospects: The 2009 Revision. New York: United Nations Population Division.
Von Hertzen, L., I. Hanski, and T. Haahtela. 2011. Natural immunity: Biodiversity loss and inflammatory diseases are two global megatrends that might be related. EMBO Reports. 12:1089–1093.
Additional Reading
Bach, JF. 2002. The effect of infections on susceptibility to autoimmune and allergic diseases. New England Journal of Medicine. 347:911–920.
Dunn, R. 2012. Letting biodiversity get under our skin. Conservation Magazine 13(3): 16-21. (A well written exploration of the significance of Hanski et al. 2012)
Knapp, S. et al. 2012. Phylogenetic and functional characteristics of household yard floras and their changes along an urbanization gradient. Ecology 01/2012; 93(8):S83–S98.
Levy, S. 2012. Reduced bacterial biodiversity is associated with increased allergy.Environmental Health Perspectives. 120(8):a304. (A concise summary of Hanski et al. 2012 and earlier related papers).
*Photo: parrchristy/Flickr via Creative Commons