Linking environmental nutrient enrichment and disease emergence in humans and wildlife

Abstract

Worldwide increases in human and wildlife diseases have challenged ecologists to understand how large-scale environmental changes affect host-parasite interactions. One of the most profound changes to Earth's ecosystems is the alteration of global nutrient cycles, including those of phosphorus (P) and especially nitrogen (N). Along with the obvious direct benefits of nutrient application for food production, anthropogenic inputs of N and P can indirectly affect the abundance of infectious and noninfectious pathogens. The mechanisms underpinning observed correlations, however, and how such patterns vary with disease type, have long remained conjectural. Here, we highlight recent experimental advances to critically evaluate the relationship between environmental nutrient enrichment and disease. Given the interrelated nature of human and wildlife disease emergence, we include a broad range of human and wildlife examples from terrestrial, marine, and freshwater ecosystems. We examine the consequences of nutrient pollution on directly transmitted, vector-borne, complex life cycle, and noninfectious pathogens, including West Nile virus, malaria, harmful algal blooms, coral reef diseases, and amphibian malformations. Our synthetic examination suggests that the effects of environmental nutrient enrichment on disease are complex and multifaceted, varying with the type of pathogen, host species and condition, attributes of the ecosystem, and the degree of enrichment; some pathogens increase in abundance whereas others decline or disappear. Nevertheless, available evidence indicates that ecological changes associated with nutrient enrichment often exacerbate infection and disease caused by generalist parasites with direct or simple life cycles. Observed mechanisms include changes in host/vector density, host distribution, infection resistance, pathogen virulence or toxicity, and the direct supplementation of pathogens. Collectively, these pathogens may be particularly dangerous because they can continue to cause mortality even as their hosts decline, potentially leading to sustained epidemics or chronic pathology. We suggest that interactions between nutrient enrichment and disease will become increasingly important in tropical and subtropical regions, where forecasted increases in nutrient application will occur in an environment rich with infectious pathogens. We emphasize the importance of careful disease management in conjunction with continued intensification of global nutrient cycles.

Figure 1

Representative diseases or hosts that respond to nutrient enrichment. A. Black Band Disease (BBD), a directly transmitted disease, in reef-building corals (photo courtesy USGS); B. Vector-borne pathogens, such as malaria and West Nile Virus, may be enhanced with nutrient enrichment owing to changes in mosquito production or larval habitat; C. Complex life cycle parasites, including the trematode (Ribeiroia ondatrae) that causes limb deformities in amphibians, can increase in abundance or pathology due to changes in intermediate host abundance or parasite production (photo courtesy P. Johnson); D. Noninfectious diseases such as Harmful Algal Blooms (HABs) may directly or indirectly cause a broad range of pathologies in human and wildlife populations (photo courtesy P. Glibert).

Figure 2

Select examples of how nutrient enrichment affects different types of disease conditions. A. Effects of experimental nutrient addition on black band disease in reef-building corals in the Bahamas; (Source: Voss and Richardson 2006); B. Influence of total nutrients (nutrient concentration multiplied by water volume) on survival of larval mosquitoes (Culex restuans); (Source: Reiskind et al. 2004); C. Experimental nutrient additions (N and P) indirectly increased Ribeiroia infection in larval amphibians through changes in infected snail abundance and per capita parasite release; (Source: Johnson et al. 2007); D. Trends in nitrogen fertilizer use (solid line) and the number of red tides (dashed line) reported for Chinese coastal waters through the mid-1990’s; (Sources: Smil (2001) for fertilizer use and Zhang (1994) for red tide abundance; reprinted from Glibert and Burkholder (2006)).

Figure 3

Geographic distribution of (A) estimated global patterns in total nitrogen deposition for 2005 (in mg N m⁻² y⁻¹) and (B) global distribution of the estimated risk of emerging infectious disease event. Relative risk scaled from low values (green) to high values (red). Panel (A) Adapted from Galloway et al. (2008) and panel (B) from Jones et al. (2008).