Date Published: January 31, 2017
Publisher: Public Library of Science
Author(s): Huaiyu Tian, Pengbo Yu, Ottar N. Bjørnstad, Bernard Cazelles, Jing Yang, Hua Tan, Shanqian Huang, Yujun Cui, Lu Dong, Chaofeng Ma, Changan Ma, Sen Zhou, Marko Laine, Xiaoxu Wu, Yanyun Zhang, Jingjun Wang, Ruifu Yang, Nils Chr. Stenseth, Bing Xu, Marco Vignuzzi.
Zoonoses are increasingly recognized as an important burden on global public health in the 21st century. High-resolution, long-term field studies are critical for assessing both the baseline and future risk scenarios in a world of rapid changes. We have used a three-decade-long field study on hantavirus, a rodent-borne zoonotic pathogen distributed worldwide, coupled with epidemiological data from an endemic area of China, and show that the shift in the ecological dynamics of Hantaan virus was closely linked to environmental fluctuations at the human-wildlife interface. We reveal that environmental forcing, especially rainfall and resource availability, exert important cascading effects on intra-annual variability in the wildlife reservoir dynamics, leading to epidemics that shift between stable and chaotic regimes. Our models demonstrate that bimodal seasonal epidemics result from a powerful seasonality in transmission, generated from interlocking cycles of agricultural phenology and rodent behavior driven by the rainy seasons.
Most emerging infectious diseases are zoonotic, and more than 70% of these originate among wildlife . Zoonotic disease emergence and reemergence has been hypothesized to be driven by environmental and anthropological variability at the human-wildlife interface [2–4]. However, recent reviews of our understanding of the determinants of spillover have shown that a critical knowledge-gap  exists as we lack empirically validated models of the ecological interactions between humans, wildlife reservoirs and key environmental drivers [6,7]. In order to untangle the complexity of zoonotic spillover, combined field surveillance and modeling approaches that link the contacts between humans and wildlife with disease dynamics within the wildlife reservoir are essential . However, such comprehensive investigations are still lacking for almost all zoonotic disease systems .
Public health scientists and epidemiologists are increasingly challenged to understand how environmental change and anthropogenic trends affect zoonotic disease dynamics at the wildlife-human interface [39–42]. An effective prevention and control method of zoonotic disease is required, which integrates ecological principles of animal, human, and environmental factors [2,9]. Our study of how shifts in disease ecology can be forced by environmental and anthropogenic processes sheds critical light on zoonotic dynamics and the persistence of disease . We have shown the ecological drivers responsible for the cascading effects of environmental variability on HFRS, using a mechanistic mathematical model integrating longitudinal field surveillance, environmental change and epidemiological data. Once the wildlife and virus dynamics are taken into account, a clear picture emerges of the role of environmental variability in zoonoses . We found support for intra-annual disease cycles driven by seasonal interactions between humans and wildlife, and by an environmentally induced cascade which can switch the dynamics of A. agrarius abundance between stable and oscillatory . This in turn affects seasonality in HFRS incidence. Our finding adequately explains the complexity and interrelatedness of the environmental, biological, and anthropogenic dimensions of zoonotic pathogen dynamics.