Impact of land use on emerging diseases: a One Health perspective

How do rapid changes in the world around us affect the risk of emerging diseases in people and wildlife? Olivier Restif, Lucinda Kirkpatrick, Sandra Telfer, David Redding, Harriet Bartlett, Orly Razgour, Greg Albery, and Sophie Vanwambeke report on their thematic session presented at the Ecology Across Borders event held in Liverpool, December 2021.

Despite its exceptional impact, the COVID-19 pandemic is only the latest in a long list of emerging infectious diseases that have jumped from wildlife to humans. Most zoonotic pathogens have coevolved with their animal reservoirs over millennia, causing little harm until they come into contact with a new host species that happens to be more vulnerable. Although we have long been familiar with some “repeat offenders” (e.g. influenza, plague, brucellosis), the list of emerging zoonotic pathogens has grown steadily in the past 40 years.

In response to this challenge, epidemiologists, veterinarians, ecologists and social scientists amongst others have joined forces under the “One Health” banner. Crossing traditional disciplinary barriers, this approach investigates the spread of pathogens in different species and their environment, whilst also looking for ecological and social factors that may facilitate spillover between host species. Because humans interact and interfere with ecosystems all around the world, One Health seeks to uncover which social and economic activities are making humans, wildlife and domesticated animals vulnerable to zoonotic diseases.

At the same time, our interactions with nature through land use are central to our response to other man-made challenges we face: climate change, biodiversity loss and food security. For instance, The UK government has recently announced plans to pay farmers to rewild large areas of land and restore floodplains, sparking debate about the country’s ability to produce more food to reduce its reliance on food imports.

Around the world, we are seeing two opposing trends:  deforestation and ecosystem degradation due to agricultural expansion in some regions, and reforestation and nature reserve creation in others. How do these rapid changes affect the risk of emerging diseases in people, livestock and wildlife? Will pathogens disappear with their hosts as natural habitats disappear, or will frequent contacts between species in patchwork landscapes increase zoonotic spillover? And can ecologists come up with environmental policies and strategies that  benefits human, animal and ecosystem health?

These are some of the questions addressed by an international panel of scientists last December in Liverpool, at the Ecology Across Borders conference co-organised by the British Ecological Society and the Société Française d’Ecologie et Evolution. Chaired by Dr Lucinda Kirkpatrick (University of Antwerp) and Dr Olivier Restif (University of Cambridge), our thematic session — entitled “Impact of land use on emerging diseases: a One Health perspective” — featured six talks by British, Belgian and American ecologists and was sponsored by BES Publishing and environmental consulting company ADAS.

Providing important conceptual background, Dr. David Redding (UCL) argued that the relation between biodiversity and zoonotic risk is complex and may differ according to the spatial scale and ecological context studied. In a recent study using data collected around the world, Redding and colleagues found that reservoir hosts of zoonotic pathogens were more abundant in human-modified landscapes, even though overall biodiversity was reduced.

Yet patterns of association between zoonotic pathogens and environmental variables are distorted by biases in research effort, as Dr. Orly Razgour (University of Exeter) discussed,  by presenting a systematic review of the impacts of land use changes on zoonotic diseases. Dr. Razgour highlighted important gaps in published research, for example, a dearth of studies assessing the effect of agricultural practices on wildlife hosts of zoonotic pathogens. Whereas  in contrast, urbanisation  is mostly discussed in the context of rodent and carnivore hosts, but rarely livestock.

Tackling the question of wildlife pathogens in urban environments, Dr Gregory Albery (Georgetown University) explained that,  whilst data suggests that urban-adapted mammals have more zoonotic pathogens, this is largely driven by sampling biases. Known reservoir species are tested more often than other species, particularly in proximity to human populations. Therefore, It is vital that future empirical studies be designed to correct those biases so that risk factors of zoonotic spillover can be unraveled.

A compelling case study assessing zoonotic risk across anthropogenic landscapes was presented by Dr. Sandra Telfer (Aberdeen University), who focused on  leptospirosis (an environmentally transmitted bacterial disease carried by rodents) in Madagascar.  Dr. Telfer showed how the abundance of different host species and the prevalence of different pathogenic species varied with land use in urban and rural regions. Mirroring earlier findings on mosquito-borne diseases, leptospira prevalence in small mammals was greater in irrigated rice fields, leading to higher infection exposure for rural workers, which could create a trade-off between economic development and public health.

The role of diverse land uses (beyond land cover) in generating complex patterns of zoonotic risk was illustrated by Dr. Sophie Vanwambeke (UCLouvain), in relation to tick-borne diseases.  Dr. Vanwambeke highlighted the importance of distinguishing between hazard (presence of infectious vectors), exposure (contacts with hazard) and management capacity (detecting and controlling outbreaks). For example, even though ticks are more abundant in forests, landscape fragmentation and human activities have shifted the burden of exposure into open terrain.

Following on the theme of rural interfaces for zoonotic spillover, Harriet Bartlett (University of Cambridge) compared the risk factors across livestock farming systems. Although intensive livestock farming is often blamed for amplifying the risk of zoonotic pathogens (e.g., avian influenza virus) Barlett argued that it provides other benefits. In particular, intensive livestock production tends to have higher yields, which could reduce the total land required to meet a set level of demand. This could allow for widespread sparing of land for nature whilst decreasing the interface between wildlife, livestock and humans. Barlett highlighted key knowledge shortfalls that must be bridged before we can determine which types of systems carry the least risk.

Whilst there is no simple solution to reduce spillover risk through one-size-fits-all land use policies, our thematic session advocated an integrated approach that is mindful of people’s health, biodiversity and food security. The study and management of zoonotic risk has a key role to play in the development of a truly transdisciplinary Planetary Health movement, which integrates a “One Health” perspective into the research and management of human impacts on the environment and life on Earth.

Find out more about Ecology Across Borders 2021, the British Ecological Society’s joint Annual Meeting with the French Society for Ecology and Evolution (SFE²).

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