The rapid global spread and human health impacts of SARS-CoV-2, the virus that causes COVID-19, show humanity's vulnerability to zoonotic disease pandemics. Although anthropogenic land use change is known to be the major driver of zoonotic pathogen spillover from wildlife to human populations, the scientific underpinnings of land use-induced zoonotic spillover have rarely been investigated from the landscape perspective.

We call for interdisciplinary collaborations to advance knowledge on land use implications for zoonotic disease emergence with a view toward informing the decisions needed to protect human health. In particular, we urge a mechanistic focus on the zoonotic pathogen infect–shed–spill–spread cascade to enable protection of landscape immunity—the ecological conditions that reduce the risk of pathogen spillover from reservoir hosts—as a conservation and biosecurity priority.

Results are urgently needed to formulate an integrated, holistic set of science-based policy and management measures that effectively and cost-efficiently minimise zoonotic disease risk. We consider opportunities to better institute the necessary scientific collaboration, address primary technical challenges, and advance policy and management issues that warrant particular attention to effectively address health security from local to global scales.

The linkages between land use and wildlife disease dynamics are well recognised in concept; however, the scientific underpinnings have rarely been investigated from a mechanistic, landscape-scale perspective. As a result, there is no philosophy of managing land use to minimise zoonotic disease emergence, or sufficient data to advance such a practice. An interdisciplinary applied research effort focused at the interface of landscape ecology, wildlife immunology, and disease ecology is required to develop an operational understanding of land use consequences for wildlife and human health.

Worldwide, epidemics of zoonotic disease—eg, COVID-19—have awakened policy makers and land use managers to the scarcity of information available to guide decision making aimed at protecting human health from wildlife-based zoonoses, a key aspect of global health security. The crucial need for science-based information that unpacks the causal mechanisms linking environmental stressors to zoonotic pathogen spillover has been recognised, and demands for action-informing data are being voiced globally by various policy, research, and funding entities, including the Convention on Biological Diversity’s Subsidiary Body on Scientific, Technical and Technological Advice, the Inter-governmental Science-Policy Platform on Biodiversity andEcosystem Services, and the US Agency for International Development.

Landscapes with high ecological integrity such as structural intactness and connectivity, biotic diversity and abundance, and generative trophic system relatedness and function, provide biosecurity. Any land use practice that reduces ecological integrity and resilience erodes the barriers to zoonotic spillover (figure 2). Ideally, a focus on the cascade will help to identify practical, context-specific land use metrics and measures to enhance landscape immunity, and thus reduce the risk of zoonotic pathogen spillover to humans.Minimising anthropogenic habitat fragmentation and penetration, and the perimeter of habitat edges, should be one of the first principles in landscape management to reduce wildlife zoonoses risk.71

Regarding the type and extent of human impact, the risk of pathogen spillover varies considerably by landscape condition.52,72 Penetrating the world’s large wild areas creates a set of risks, landscapes that are semi-wild with strong edge effects create a different set of risks,11 and intensely transformed landscapes with high human population density present even greater risks.73 Thus, a practical approach is required to organise conservation and distancing measures aimed at sustaining landscape immunity using the Three Global Conditions for Biodiversity Conservation and Sustainable Use framework.

Raina K Plowright*, Jamie K Reaser*, Harvey Locke, Stephen J Woodley, Jonathan A Patz, Daniel J Becker, Gabriel Oppler, Peter J Hudson, Gary M Tabor