Introduction

Climate change has resulted in a significant increase in temperature, precipitation, humidity, and the frequency and intensity of storms [1–3]. These environmental changes have especially optimized the conditions for the emergence and spread of vector-borne neglected tropical diseases (NTDs) into novel regions of the world [1,2]. The increased emergence of NTDs due to this worldwide spread of such vectors should not be underestimated. The tiger mosquito (Aedes albopictus) can transmit many different types of arboviruses such as dengue fever, yellow fever, and West Nile virus, as well as nematode-borne parasitic diseases [4,5]. Phlebotomine sandflies are a vector of leishmaniasis. Under the complex effects of climate change, modelling the spread and annual cycling of these vectors has required additional hydrological and ecological data [6].

However, one underinvestigated aspect of these changes is the influence on landscapes and soils as vector habitats. It is possible that improved habitat conditions may enhance the emergence and spread of these vector-borne NTDs. If so, investigating relevant soil characteristics may improve models, identify novel areas of concern, and suggest land management practices to mitigate the spread of NTDs. It may be possible that soils that hinder the spread of disease are “healthy” soils, and soil health, like public health, can be improved and managed. Likewise, improved characterisation of regions at risk can better inform public health policy. To illustrate for the NTD community the role of soil in the spread of disease, we examine the concept of soil health and then consider the implications for example NTDs and vectors.

Soil health

Soil health is generally defined in terms of ecosystem services (benefits of nature to humans), such as water retention, nutrient cycling, and supporting plant life [7]. Physically healthy soils are well aerated and have balanced moisture content. Fertile soils are high in organic matter and are abundant in plant nutrients. Chemically healthy soils are of moderate pH and not contaminated or saline. Finally, microbiologically healthy soils consist of diverse communities that efficiently cycle nutrients, form beneficial symbiotic relationships with plants, and suppress pathogens. Yet does climate change affect soil health in a manner that promotes the spread of NTDs? Is it possible to consider resistance to disease as a soil ecosystem service? Do the key soil characteristics vary by vector or disease? Identifying the soil health factors affecting the spread of NTDs (Fig 1) may be the key to their mitigation and prevention.

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Fig 1. Soil health factors affecting the spread of NTDs.

Standing water for breeding is a result of poor soil structure (A) and salinization (B) and can be enriched with organic matter and nutrients through soil erosion (C) interacting with poor organic matter (D) and fertilizer (E) management. Soil-dwelling vectors are affected by organic matter management (D) and the microbiome composition of the soil (F).

https://doi.org/10.1371/journal.pntd.0011378.g001

Mosquito-borne diseases

There are numerous mosquito-borne diseases where newly formed ideal habitat conditions (i.e., increased precipitation, standing water, and eutrophication) have resulted in the emergence and spread of NTDs [6]. For this reason, dengue fever cases have been reported to increase in Taiwan, Australia, Mexico, Thailand, Peru, and other nations [6]. There are 3 key soil characteristics related to the formation of such habitats.

Sandfly-borne diseases

Phlebotomine sandflies reproduce in caves, human-made structures, and soil cervices, and larvae develop in humid, organic matter–rich environments [13]. This vector is particularly sensitive to human land use changes [1]. The increased emergence and spread of sandfly-borne diseases like leishmaniasis has also been linked to increases in temperature (increased metabolic activity accelerating the life cycle) and rainfall (greater availability of breeding sites) [1]. Soil and near-soil dwelling vectors are dependent on 2 major soil characteristics.

Soil-transmitted helminths

Land management for soil-based NTDs may be more challenging than soil-based vectors, because favourable conditions for crops and natural areas (high OM, moist soils, and available nutrients) may also benefit soil pathogens and other NTDs. For example, it is predicted that with increased soil humidity due to climate change, soil-transmitted helminth (STH) survival and spread will be enhanced [15]. As moist soil environments are especially important at the egg and larval stages to prevent desiccation [15], soils with high water retention capacity (fine-textured, high OM) are more likely to support STHs. However, especially in drought-prone regions, crop performance is often greatest on such soils. Avoiding use of contaminated irrigation water or manure, as well as modifying irrigation methods to limited prolonged saturated conditions, may be strategies to reduce soil-based NTD risk.

Next steps

By considering physical, chemical, fertility, and microbiological characteristics of soil health, we may be able to better identify areas of concern related to the development and spread of NTDs. In addition to being an underrecognized reservoir for the production and spread of NTDs, unlike climatic factors, soil health can be actively managed to promote ecosystem services, which mitigate the spread of NTDs. By identifying key regions of concern where soil services are degraded, we can link land management to public health policy. Soil scientists, land managers, agronomists, farmers, and others are in a unique position to assist healthcare professionals in the fight against NTDs. Proactive, region-wide steps to simultaneously improve soil and human health are vital in light of climate change. The result can be increased agricultural yields and economic benefits, conservation of natural areas and resources, locally adapted drugs and therapies, and resistance to the spread of NTDs.