Towards a 'people and nature' paradigm for biodiversity and infectious disease

Abstract

Zoonotic and vector-borne infectious diseases are among the most direct human health consequences of biodiversity change. The COVID-19 pandemic increased health policymakers' attention on the links between ecological degradation and disease, and sparked discussions around nature-based interventions to mitigate zoonotic emergence and epidemics. Yet, although disease ecology provides an increasingly granular knowledge of wildlife disease in changing ecosystems, we still have a poor understanding of the net consequences for human disease. Here, we argue that a renewed focus on wildlife-borne diseases as complex socio-ecological systems-a 'people and nature' paradigm-is needed to identify local interventions and transformative system-wide changes that could reduce human disease burden. We discuss longstanding scientific narratives of human involvement in zoonotic disease systems, which have largely framed people as ecological disruptors, and discuss three emerging research areas that provide wider system perspectives: how anthropogenic ecosystems construct new niches for infectious disease, feedbacks between disease, biodiversity and social vulnerability and the role of human-to-animal pathogen transmission ('spillback') in zoonotic disease systems. We conclude by discussing new opportunities to better understand the predictability of human disease outcomes from biodiversity change and to integrate ecological drivers of disease into health intervention design and evaluation.This article is part of the discussion meeting issue 'Bending the curve towards nature recovery: building on Georgina Mace's legacy for a biodiverse future'.

Keywords: biodiversity; disease ecology; epidemiology; global change; infectious disease; socio-ecological systems.

Figure 1.

Local social–ecological feedbacks generate and reinforce infectious disease risks. Human zoonotic and vector-borne disease risks (blue triangle) arise from the convergence of circulating pathogen hazards within local ecosystems (shaped by host and pathogen diversity and prevalence), drivers that create opportunities for exposure (e.g. agricultural activities, urbanization and infrastructure, land conversion, wildlife hunting, hydrometeorological extremes) and individual- and population-level factors that influence vulnerability to disease and epidemics (e.g. individual physical condition and immunity; health systems access and functionality; inequality and social cohesion). Although often discussed and studied as separate phenomena [17], these processes are interdependent and subject to numerous feedback effects (orange arrows and text) that can generate or reinforce disease risks. For example, a high burden of disease (hazard) can impact community livelihoods and poverty (vulnerability), leading to increased reliance on local environment, land use or wildlife (exposure), which in turn can further impact local ecological communities (hazard). All these local processes are shaped by global forces, including unequal and extractive power relations, climate change and biodiversity degradation (yellow boundary), which can simultaneously impact pathogen hazards, exposure processes and vulnerabilities.

Figure 2.

Compositional shifts in host and disease diversity under intensifying land use. Increasing intensities of anthropogenic land use intensity, from minimally disturbed habitat to rural ecosystems, towards high-intensity agriculture and urbanization, are generally associated with declines in overall local biodiversity (top graph). This overall trend masks compositional shifts in host and arthropod vector diversity that can significantly alter the local diversity and burden of zoonotic and vector-borne disease (ZVBD; middle and bottom graphs), including losses of more human-sensitive taxa (and their specialist pathogens; red line), the rise of highly synanthropic species (yellow line) and variable or hump-shaped responses of other species (blue line). These community shifts will reshape local disease transmission ecologies and create differences in disease diversity and burden in different types of landscape (examples in bottom graph captions). A deeper understanding of these changes in host, vector and pathogen diversity in response to human pressures at the level of biomes or ecoregions—for example, through leveraging global biodiversity data—may facilitate prediction of the infectious disease consequences of biodiversity change for many under-studied pathogens (see §6).