1 The health impact of agricultural development
Modern human populations are dependent on agriculture. It is a crucial part of our food systems, playing a key role in providing food security for our growing population. Industrial agricultural systems, despite generating negative impacts on some fronts, still supply global markets with large volumes of food and have boasted breakthroughs in crop productivity, food processing, distribution and improvements in food safety (Frison 2016). On the other hand, in low-and-middle-income countries, small-scale agriculture in rural communities provides sustenance, shelter, medicine, and income, thereby reducing hunger and poverty and improving livelihoods. Through these means, agriculture can create a pathway to improve the health and livelihoods of the poor. The positive impacts of agriculture on human health are far-reaching; from nutrition to economic development leading to improved access to healthcare (Hawkes and Ruel 2006a). These processes by which agriculture can improve human health tend to be those which are highlighted and focused on by the agricultural sector. There are, however, negative impacts on health created by agriculture and agricultural development, whereby agriculture also puts human health at risk (Hawkes and Ruel 2006a; Lines et al. 2020).
Unintended side effects of agriculture can impact negatively on human health, through processes such as disease transmission, occupational health hazards, and malnutrition (Hawkes and Ruel 2006b). In many cases, agriculture is associated with increased risk of infectious disease transmission, where agricultural drivers of transmission have been attributed to >25% of all infectious diseases which have emerged in humans (Alexandratos and Bruinsma 2012). These links between agriculture and poor health can reduce the productivity of farming communities where agricultural workers in ill health are less able to work. This in turn can jeopardize food security, income and economic development (Hawkes and Ruel 2006b), creating a barrier to the pathway out of poverty and undermining the benefits which agriculture provides to poor communities (Lines et al. 2020). There is a tendency in the agricultural sector to focus on the positive impacts which it has on health, with the processes producing negative health impacts being accepted as a ‘necessary evil’, or an inevitable by-product or trade-off of useful agricultural activities (Lines et al. 2020).
One such unintended negative consequence is increased vector-borne disease (VBD) risks due to agricultural practices. Tropical and low-and-middle-income countries bear a disproportionately high burden of VBD s, and also house an estimated three-quarters of global agricultural land cover (World Bank 2022; Wilson et al. 2020). The mechanisms through which agriculture can drive changes in VBD s are complex and often poorly understood, making them difficult to control for and manage when planning agricultural projects (WHO et al. 1996). Agricultural development can disrupt ecological and social systems through many mechanisms, leading to changes in VBD transmission. Land-use and land-cover changes for agriculture alter environmental conditions and subsequently can impact vector ecologies (Ferguson et al. 2010; Foley et al. 2005; Fornace et al. 2021; Jones et al. 2013). A common example of this is the creation of suitable breeding conditions for disease vectors by irrigation schemes for agricultural projects (Norris 2004; Patz et al. 2000). Changes in the local economy and human demographics driven by agricultural development can also impact population exposures and vulnerabilities to VBD s. Examples of this include the monetary gains of agricultural production leading to agricultural communities having improved access to healthcare, and better infrastructure and protections against vectors (WHO et al. 1996). Agricultural intensity generally rises with population density (Boserup 1965). The global population is projected to increase by around one-third by 2050, requiring a 70% increase in food production (FAO 2002). Agricultural intensification and expansion to support this growth will be fundamental for sustenance (Rohr et al. 2019). Current trends suggest that this expansion will likely lead to changes in VBD transmission. In the agricultural sector, plans for ‘Sustainable Intensification’ are at the forefront of agricultural development. Sustainable Intensification aims to create agricultural systems and methods which will increase agricultural yields to feed growing populations, while mitigating adverse impacts on the environment (Wezel et al. 2015). So far, however, these plans do no take mitigation of negative health impacts from agriculture into account.
As the agricultural sector develops to cope with changes in human populations, the environment, and the climate through Sustainable Intensification, it is imperative that VBD s are also considered. We must find effective ways to achieve high agricultural productivity without the unintended negative health costs from VBD s, and incorporate these methods into plans going forward (Lines et al. 2020). One of the major barriers to this goal currently is a lack of ownership of the problem. As the responsibility for disease surveillance, control and mitigation traditionally falls on the health sector, the agriculture sector tends not to be involved in these processes, despite the often deadly impacts of agriculture on disease ecology (Chan et al. 2022a). In some instances, in order to improve economic efficiency, agricultural development projects do include health components to mitigate sick labour (e.g. providing bed-nets, rapid diagnosis and treatment to agricultural workers in malarious settings (Packard 1986)). However, these ‘downstream’ solutions are not adequate. Instead, the agricultural sector needs to take accountability and take part in ‘upstream’ prevention. To do this, alliances between health and agriculture sectors are required to share the burden of mitigating and building out VBD risks created by agriculture through new methods which optimize the benefits of agriculture, while minimizing the risks on health (WHO et al. 1996; Lines et al. 2020). ‘Adaptation co-benefits’ have been described as a crucial step to break down such sectoral silos to allow for climate-resilient agricultural development. These are adaptations or developments to agricultural methods or policies which have a socially, economically or environmentally desirable outcome (Crumpler and Meybeck 2020). We believe that the definition of co-benefits can be expanded to include health outcomes, especially those linked to vector-borne disease transmission.
In this chapter, we aim to highlight the connections between agriculture and VBD, and to encourage collaborative disease and agriculture related research, planning and policy which can improve agricultural production while reducing risks to human health from VBD. We will provide an overview and examples of the common mechanisms by which agriculture impacts VBD transmission, then introduce the co-benefits approach and how it could be used to find ‘win-win’ solutions to the challenge of agriculture and VBD. The current barriers to overcoming this challenge will be outlined, with suggestions for both the agriculture and health sectors for how to overcome them in the future.
2 Drivers of agriculture-vector-borne disease associations
There are many driving forces which can increase or decrease VBD risks associated with agriculture and agricultural development. These drivers can be placed in three broad categories: socio-economic, demographic and environmental.
2.1 Socio-economic drivers
2.1.1 Economic
The economic drivers of agricultural impact on VBD are broadly linked to the improvements in conditions and quality of life which agriculture can offer through providing economic benefits. Poverty can enhance vulnerability to VBD s, primarily by limiting people’s ability to manage and address health risks (Bardosh et al. 2017; Blas and Kurup 2010). It is the general consensus that socio-economic impacts in the wake of agricultural development follow a positive trend, where VBD risk and incidence is ‘built-out’ through local improvements to infrastructure, better access to health services and increased protection against vectors (WHO et al. 1996). Such positive impacts will in turn influence the health and well-being of the agricultural community, generating a positive feedback loop resulting in further improvements to the agricultural and economic productivity of the workforce (WHO et al. 1996).
Although there are many instances of agricultural development increasing wealth and hence improving health, they are rarely documented due to its indirect nature. Nonetheless, one example is the ‘paddies paradox’ hypothesis, which was used to partly explain why, until the early 2000s, there was often less malaria in African rice-growing villages despite higher numbers of mosquitoes in these areas (as rice paddies provide an ideal breeding environment for malaria vectors). Ijumba et al. (2001) argued that residents of rice-irrigation schemes became wealthier from their agricultural productivity, and part of this wealth trickles down into their health, by providing access to bed-nets and antimalarials to counter the higher vector abundances. However, this paradox may no longer be valid these days because malaria interventions have become more equitably distributed across Africa (Taylor et al. 2017). Upon a re-assessment of the paradox, Chan et al. (2022b) found that, compared to non-rice-farming communities, irrigated rice communities are now more exposed to greater malaria risk. This should be of concern to the agricultural sector as it plans to scale-up rice production across the continent.
2.1.2 Demographic
Agricultural development can often drive demographic changes which put populations at increased risk of ill health due to VBD. Large agricultural projects can create a demand for labor, resulting in the movement of populations of human workers. The migration of large groups of people with differing levels of immunity into new areas can pose VBD risks through two broad mechanisms. Firstly, an influx of previously unexposed people to an area with high or endemic disease transmission leaves them exposed to infections which have potential to be severe or fatal due to their naïve immunity (Prothero 2001; WHO et al. 1996). Ethiopia saw mass forced-resettlement schemes during the mid-80s. People without malaria immunity were moved from the northern plateau to lower lands where malaria is endemic, and were subsequently exposed to risks of high mortality and morbidity, further enhanced by exposure to higher vector abundances for those resettled to irrigation schemes (Kloos 1990; Prothero 2001). Secondly, human migration can introduce or reintroduce pathogens from other settings. Once a capable vector can transmit the introduced pathogen, this can lead to outbreaks in the workforce and in non-immune local communities. An example of this is the reintroduction of malaria to Eswatini in the 1960s and 1970s. Successful control measures (DDT spraying) had effectively eradicated malaria from the area by 1959, but a resurgence of malaria was driven by re-introduction of Plasmodium parasites to the area by migrant workers from malaria-endemic areas of Mozambique to work on sugarcane estates (Packard 1986; Martens and Hall 2000). As a more recent example, it has been shown that cross-border migrant workers play a role in spreading multidrug resistant malaria at the Thailand-Cambodia and Thailand-Myanmar borders (Bhumiratana et al. 2013; Tangena et al. 2016; Wangroongsarb et al. 2012).
These issues of VBD transmission and illness are often exacerbated by environmental and socio-economic drivers of disease which impact migrant workforces. Many crops which are cultivated in large agricultural schemes create a seasonal demand for temporary agricultural workers. This often occurs during or soon after the rainy season when VBD transmission is at its most intense (Wangroongsarb et al. 2012). These populations are often poor and marginalized groups who are subject to poor health infrastructure, inadequate basic services and vector control in housing (Prothero 2001).
2.2 Environmental drivers
Agriculture and agricultural development induce environmental and ecological changes which can often impact one of the variables which determine vectorial capacity. Examples of such environmental and ecological changes brought about by agricultural development include the creation of new breeding sites for vectors; changes in species dynamics; changes in microclimatic conditions which may favor vector longevity; and increases human-vector contact (Wangroongsarb et al. 2012). For brevity, we will focus on two major environmental drivers, irrigation and deforestation, though many others exist.
2.2.1 Irrigation
One of the most important ways in which environmental changes caused by agricultural development impact VBD is through water redistribution. Irrigation networks, dams and reservoirs increase with agricultural development and these changes in water distribution are widely associated with increases in disease vectors and hosts of human pathogens (Hawkes and Ruel 2006b). There exists a wealth of scientific literature highlighting how irrigation projects for agricultural development can induce changes in vector bionomics, species diversity, and disease transmission.
Through providing ideal habitats for the freshwater snail vectors, dam building has led to the introduction of schistosomiasis to previously unexposed populations (Mutero et al. 2006). Snail vectors had never been reported in the Hola settlement scheme in Kenya prior to an irrigation scheme in the 1950s. The following decade, a 70% prevalence of schistosomiasis was reported within the population, which rose to 90% by 1982 (Mutero 2002). In central Tunisia, the construction of irrigation facilities alongside unusually high temperatures created ideal conditions for an increase in leishmaniasis vector Phlebotomine sandflies. These changes have been linked to increases in human visceral and cutaneous leishmaniasis (Salah et al. 2000). Irrigated rice agriculture has been notoriously linked to malaria vector production, with rice fields acting as a major source of the primary malaria vector species in central China, sub-Saharan Africa, parts of central Asia, Indonesia, and Peru (Lacey and Lacey 1990). Ultimately, rice-growing areas in sub-Saharan Africa often harbour high malaria transmission capacity (Haileselassie et al. 2021; Chan et al. 2022b). In Sri Lanka and the Thar Desert in India irrigation development has been linked to both increases in malaria vectors and changes in malaria transmission from mild to frequent epidemics (Amerasinghe and Ariyasena 1991; Tyagi and Chaudhary 1997).
2.2.2 Deforestation and plantations
The clearing of land for agricultural activities is the largest single cause of deforestation (FAO 2022). Deforestation alters the ecology of a landscape, impacting temperature, humidity, vegetation, water retention, and soil composition. Disease vectors are sensitive to such changes, and thus, deforestation and the knock-on effects it has on a landscape’s ecology influence the transmission of VBD s through changes in vector ecology, alongside human behavior patterns (Yasuoka and Levins 2007).
Deforestation has been shown to increase the risk of scrub-typhus in Korea, and agriculture-related work activities have been shown as risk factors transmission (Kim et al. 2018; Ma et al. 2017; Min et al. 2019). This is driven by the secondary growth of scrub vegetation after deforestation which provides an ideal habitat for the mite vectors, resulting in higher vector densities (Min et al. 2019). The distribution of lymphatic filariasis is impacted by deforestation and agriculture, and may be linked to the generation of suitable vector habitats (Duker and Kwarteng 2021), with many of the important mosquito vectors of lymphatic filariasis shown to be positively associated with deforestation (Burkett-Cadena and Vittor 2018). In southwest Nigeria, lymphatic filariasis was found to be higher in communities with lower canopy height and tree coverage (Brant et al. 2018). In south-east Cote d’Ivoire, the abundance and distribution of Aedes vectors of lymphatic filariasis were found to be impacted by landcover and landuse change from rainforest to oil palm plantations (Zahouli et al. 2017). In the Democratic Republic of Congo, deforestation and agricultural expansion were associated with increased indoor biting rates of malaria vectors, causing an increase in malaria prevalence in children (Janko et al. 2018). Increases in the human incidence of the simian malaria Plasmodium knowlesi has been shown to be strongly associated with deforestation in Sabah, Malaysia (Fornace et al. 2016, 2019b). Deforestation and land-use change for agriculture have been linked to changes in the reservoir macaque behavior and increased contact between people and mosquito vectors and forest edges, and the creation of favorable vector breeding habitats (Byrne et al. 2021; Fornace et al. 2019a; Stark et al. 2019).
Deforestation activities are often the first steps in the creation of plantation farms. In recent decades monoculture-based agriculture for crops such as oil palm and rubber have expanded extensively, especially in South East Asia (Ahrends et al. 2015; Bartholomé and Belward 2005; Shah et al. 2019; Tangena et al. 2016). Here, multiple studies have shown increases in these two agriculture types to be associated with outbreaks and increases in prevalence of VBD s such as dengue, malaria and chikungunya (Morand and Lajaunie 2021; Shah et al. 2019). Monocultures tend to have lower species richness compared to primary and secondary forests and altered ecology in terms of canopy, undergrowth, humidity, greater human disturbance (Shah et al. 2019). Rubber plantations provide suitable environments for long-lived forest vectors such as Anopheles dirus sensu lato malaria vector and Aedes albopictus dengue and chikungunya vectors (Jomon and Valamparampil 2014; Sulaiman and Jeffery 1986), and create a wide range of man-made and natural larval habitats (Tangena et al. 2016). Multiple epidemics of dengue and chikungunya have been reported from plantations in Malaysia and India in the past two decades, each occurrence infecting thousands of people in plantation working communities (Kumar et al. 2011; Nakhapakorn and Tripathi 2005; Tangena et al. 2016). Regular malaria outbreaks have been reported across Southeast Asia in rubber plantations and other monocrop plantations. Yasuoka and Levins (2007) describe changes in vector composition increasing malaria transmission among cassava and sugarcane plantation workers in Thailand. The initial development of the plantations led to decreases in the shade-loving vector Anopheles dirus, however the species was replaced by the sun-loving vector Anopheles minimus.
It is important to note that the impact of deforestation on VBD transmission is complex and not uniform in every setting, as it depends on many factors involved in different vector ecologies and disease transmission cycles (Kalbus et al. 2021). In some African settings deforestation can actually lead to reductions in malaria transmission by reducing suitable habitats of forest dwelling vectors (Guerra et al. 2006). Additionally, to our knowledge no positive association has yet been shown dengue and deforestation, although studies are sparse (Husnina et al. 2019). Broadly speaking however, a systematic review by Burkett-Cadena and Vittor (2018) has shown that the net effect of deforestation favors human disease vectors, and that non-deforested forest habitats favor non-vectors.
2.3 The complexity of drivers
We have highlighted that the impact of agriculture and agricultural development on VBD transmission can be driven by multiple drivers and varying mechanisms working within them. These drivers do not work in isolation and are often working in conjunction with each other. In Lowland Eswatini, malaria had been successfully controlled, prompting the expansion of sugarcane agriculture. This required the construction of irrigation schemes, providing a niche for Anopheles vectors to breed in, resulting in resurgences in malaria (Packard 1986). These resurgences were intensified by poor infrastructure and frequent importation of migrant labourers from endemic-Mozambique (Tejedor-Garavito et al. 2017). This example highlights how the environmental, socio-economic and demographic drivers can overlap to exacerbate the negative impacts of agricultural development on VBD transmission. Another example is the Mahaweli rice development project in Sri Lanka, where irrigation created breeding sites for Japanese encephalitis virus (JEV) vector Culex tritaeniorhyncus, resulting in increases in human-vector contacts (Amerasinghe and Indrajith 1994). A separate agricultural development project nearby encouraged pig production, which are the reservoir host for JEV. Subsequent JEV epidemics severely impacted the newly settled and non-immune communities of agricultural workers (Mutero et al. 2006).
When there are multiple drivers of transmission working at varying scales, untangling the cause-effect relationship of agriculture on VBD transmission becomes a hugely complex task. Showing that there is a relationship between an agricultural activity and disease transmission is the first step, but understanding the mechanisms underlying this relationship would require multiple robust field studies and analyses. In order to translate this knowledge into policy change or change which will be accepted within the agricultural sector, further studies and trials to develop ‘win-win’ solutions, or co-benefits, for agriculture and health need to be found.
3 Co-benefits: the concept
By definition, a co-benefit is an additional benefit from an action or intervention that is undertaken to achieve a particular purpose. It implies a ‘win-win’ strategy to address multiple goals with a single policy, and can be implemented across different scales and sectors (Crumpler and Meybeck 2020). The term emerged in the 1990s and is popular amongst the climate change community (Mayrhofer and Gupta 2016). A classic example of a climate co-benefit is reducing fossil fuel combustion, which not only helps tackle climate change but also improves air quality and thus has significant health and environmental benefits. In contrast to co-benefits, an intervention can sometimes create conflicts or trade-offs, which need to be taken account of and minimised.
Whilst co-benefits can arise from climate change adaptation in agriculture, this term can be extended to not only cover climate actions but also agricultural interventions. Health co-benefits which are generated by agricultural development strategies exist, but these are often unintended positive side effects, similar to the aforementioned unintended negative side effects. More effort needs to be placed in recognising, developing, and adopting co-benefits with intended positive side effects. This is especially important as discussions at the agriculture-health interface currently place a lot of emphasis on trade-offs, rather than co-benefit solutions.
4 Agriculture-vector-borne disease co-benefits: case studies
Co-benefits, a new term at the interface between agriculture and VBDs, aims to optimise health and productivity benefits of agriculture, whilst minimising the health risks to the agricultural community. To provide better understanding of this new term, we will highlight a number of case studies, largely in the context of irrigation, rice and mosquito-borne diseases.
4.1 Irrigated rice: water management techniques
Irrigated rice is typically grown in fields which are continuously flooded from transplanting to around one week before harvest. Providing a constant flow of water can increase rice productivity, not only because rice is a water-loving plant but also because water helps control competition from weeds. Unfortunately, this stable body of water, continuously present for at least 3–4 months (depending on variety), permits many cycles of mosquito vector breeding. Consequently, irrigated rice cultivation in many parts of the world (sub-Saharan Africa, Asia and South America) are associated with increased transmission of mosquito-borne diseases such as malaria, Japanese encephalitis, lymphatic filariasis and zoonotic arboviruses (Lacey and Lacey 1990). Whilst medical entomologists have been advocating alternative water management techniques such as intermittent irrigation to control vector proliferation, these techniques are often not taken up by farmers as they do not necessarily produce greater yields (Van der Hoek et al. 2001; Keiser et al. 2002). There are several exceptions, which include intermittent irrigation in Peru and China, both of which are model examples of co-benefits.
In north-western Peru, intermittent irrigation was applied to rice crops in four regions by the National Institute of Agrarian Innovation, under an agreement with the Ministry of Health (FAO). Although farmers were hesitant to change their practices at first, they were incentivised by the reflected 20–25% increase in crop yields and 26–57% water-saving capabilities (RTI International 2012). In terms of its health co-benefits, intermittent irrigation in rice was not only able to reduce malaria vector production by 70–93% but also reduced malaria transmission and the number of outbreaks (Chang 2007).
Irrespective of mosquito production, agronomists in conjunction with climate change scientists have also been developing water-saving technologies as water for agriculture is becoming increasingly scarce. Alternate wetting and drying irrigation (AWD) is another variation of intermittent irrigation which was implemented in numerous Asian countries including Vietnam, Bangladesh and Thailand. Its benefits are diverse: reduced greenhouse gas emissions, improved soil structure, greater yields, reduced environmental impact and increased farm efficiency (Allen and Sander 2019). Whilst their effects on mosquito production and VBD (namely Japanese encephalitis) transmission have not been explored, it is suspected that AWD can disrupt mosquito life cycles and hence reduce vector abundance in rice areas (Allen and Sander 2019).
System of rice intensification (SRI) is a package of management methods concerning soil, water and nutrients to increase the productivity of rice whilst saving water and seed requirements. As intermittent irrigation (or AWD, used interchangeably) is part of this package, SRI also has the potential to reduce vector densities in rice fields (Mati et al. 2021). Only one study has been conducted so far, in an irrigation scheme in Kenya, and observed that larvae were completely eliminated following two days of drying (Omwenga et al. 2014).
Another water management technique in rice cultivation which can potentially bring co-benefits is drip irrigation. By precisely watering plants or small planted areas directly, drip irrigation is highly effective in water productivity whilst reducing greenhouse gas emissions and other negative environmental effects such as groundwater pollution (Tas 2021). Without any standing water, mosquito vectors would not be able to develop.
By limiting mosquito development, these water management techniques (AWD, intermittent irrigation, SRI and drip irrigation) do not only mitigate problems in water scarcity but also malaria risk.
4.2 Irrigated rice: nutrient management techniques
Various studies have shown that the application of synthetic nitrogenous fertilisers in rice fields is associated with increased mosquito populations, possibly through increased nutrients for larval development or reducing water turbidity and hence increasing attractiveness for oviposition (Mutero et al. 2000, 2004; Victor and Reuben 2000). However, with very few exceptions, fertiliser application cannot be avoided; it is necessary to increase rice productivity. Whilst synthetic chemicals are primarily used, organic materials such as neem, Azolla, manure and biochar are viable options that may also provide climate co-benefits by reducing the amount of greenhouse gas emissions.
Recognising the necessity of fertilisers and their frequency and timing of application, Tanzanian malariologists tested combining fertiliser application with biolarvicides (Bti). This was highly effective in reducing mosquito larval densities (An. gambiae s.l. and Cx. quinquefasciatus), reaching up to 78.9% reduction (Mazigo et al. 2019b). This agricultural-VBD intervention provides co-benefits by improving rice grain output whilst reducing malaria transmission. Moreover, social science studies have revealed that willingness to contribute to and adopt this fertiliser- biolarvicide within their practices were high amongst farmers (Mazigo et al. 2019a).
Neem (or Azadirachta indica) is a natural extract that has many uses in a farming system: pest and insect control, animal feed, and fertilisers. Its insecticidal properties work indirectly, where it acts as an anti-feedant, repellent and egg-laying deterrent and eventually causes insects to starve to death (Benelli et al. 2015; Nicoletti et al. 2016). Neem cake is often used as an organic fertiliser by providing nitrogen and phosphorus. Given these co-beneficial properties, neem has been tested in rice fields for its efficacy against mosquito vectors and in enhancing grain yield. Laboratory trials have demonstrated that neem, including leaf extracts, are effective against malaria vectors, through repellence, oviposition deterrence, preventing adult emergence and reducing Anopheles survival (Vatandoost and Vaziri 2004; Nathan et al. 2005; Elsiddig 2007). In rice fields, neem cake powder enhanced grain yield, resulting in a greater number of productive tillers, plant height and grains per panicle, all whilst significantly reducing culicine mosquito vectors (Rao et al. 1995).
Like neem, mosquito fern (or Azolla) can have diverse benefits in a farming system too: as a biofertiliser, livestock feed and, sometimes, mosquito control. They occur naturally and in large quantities in rice fields. As an agricultural input, it is a source of green manure due to its symbiotic relationship with nitrogen-fixing cyanobacteria, and hence enhances the fertility of rice paddy soil. It has also been proposed as a way to promote carbon sequestration (Kollah et al. 2016). When grown into a thick carpet on the surface, Azolla can act as mosquito control by making it difficult for larvae to breathe and interfering with oviposition (IRRI 1988). In India, when Azolla covered more than 80% of the water surface, it was found to significantly reduce immature mosquito populations. Unfortunately, since such coverage can only be achieved two weeks after transplanting, its usefulness to control the early peak in vector production (in the 5–6 weeks following transplanting) is limited (Rajendran and Reuben 1991). However, because vector production is not restricted to the initial post-transplanting period, it can be useful during other rice-growing phases. At the farmer level, Azolla is beneficial as it keeps soil moist, reducing the labour and cost necessary for weeding and increasing grain yield by 9–14% at virtually no cost (Lines et al. 1992). However, Azolla can be labour intensive, where farmers may not have any economic advantage in choosing it over chemical fertilisers.
4.3 Rice-fish/duck co-culture systems
Fish provide a multitude of co-benefits when introduced to a rice system. They generate higher economic return by providing an additional source of income and minimising use of additional fertilisers, in turn increasing rice growth and yield. In some settings, they also generate fewer mosquito vectors. In a meta-analysis on malaria vector control in experimental rice fields, rice-fish co-culture reduced anopheline immatures by 82–87% (Chan et al. 2022a). Rice systems are not only limited to one species of fish; herbivorous fish have been released in combination with larvivorous fish to complement them by consuming aquatic weeds which would otherwise obstruct larvivorous fish movement. In one such study, this combination allowed 75–82% suppression of larvae, including the first 3–5 weeks after transplanting when peak mosquito production occurs. Nonetheless, more research is required to optimise using fish as vector control, as more than 100 fish species eat mosquito larvae, so species must be carefully selected for rice fields to ensure these co-benefits (Lacey and Lacey 1990).
Popular in China, rice-fish cultivation had increased from 11 provinces in the 1980s to 25 provinces by the 2000s. This expansion in rice-fish system use was not only correlated with a significant decrease in malaria vector abundance, but also in malaria incidence1 (Zhao and Xue 2022). To our knowledge, rice-fish systems have only been trialled once in sub-Saharan Africa, in a study which found that Tilapia was effective not only as a food and protein source but also in suppressing An. gambiae s.l. by 88% (Bolay et al. 1990). Mosquito control using rice-fish co-culture in Californian rice fields were less evident, possibly due to the fish species and their feeding preferences (omnivorous or preference for predators)(Blaustein 1992; Kramer et al. 1987). Nonetheless, many studies saw a net profit in rice-fish systems over rice-only systems, up to 2.5 times (Victor et al. 1994).
Integrated rice-duck farming (IRDF) has been extensively explored in East Asian countries. Various studies have reported higher rice yields of 10–20% compared to traditional rice systems. Ducks did not only control weeds and insect pests very effectively, they also provided an additional source of income for farmers (Hossain et al. 2005; Pernollet et al. 2015). Moreover, climate change researchers had found that by significantly reducing methane emissions, IRDF can mitigate global warming potential (Xu et al. 2017). In China, ducks were also seen to forage on mosquito larvae, achieving 92–99% mosquito control (Zhao and Xue 2022). With this multitude of transectoral benefits (increased food security, climate change mitigation, income generation), the potential of IRDF as malaria vector control is worth further exploration, especially in African rice fields.
Nowadays, in China, other rice co-culture systems are being explored, such as combinations of rice with crab, crayfish, turtle, frog and/or shrimp.
4.4 Wet-crop dry-crop rotation
Practising crop rotation provides many benefits to a farmer, both economically and socially. It diversifies the array of crops or products, avoids build-up of resistance of insects, pathogens and weeds, and spreads labour demand, which allows equipment costs to reduce. Studies on the rotation of rice fields and dry-crop fields by alternating seasons and its effect on anopheline larvae have only been documented in China. The review by Zhao and Xue (2022) provide a summary of wet-crop dry-crop rotation, demonstrating its ability to increase crop productivity, whilst reducing vector breeding and hence malaria incidence. For example, Gao et al. found that biannual rotation of rice fields with dry fields (wheat or rapeseed) changed vector breeding sites significantly, reducing An. lesteri and An. sinensis densities around 93–100% (Zhao and Xue 2022). Another study found that vector breeding was also reduced when rice fields were left fallow throughout winter (Qunhua et al. 2004).
4.5 Aquaculture in dams
Whilst dams are crucial for agricultural and economic development, they can also increase the transmission of VBD s such as schistosomiasis. To promote co-benefits in equity, health, sustainable development and climate resilience, Lund et al. proposed several agricultural innovations based in sub-Saharan African dams (Lund et al. 2021). The first is the introduction of the African river prawn to target schistosomiasis-infected snails and thus reduce human disease prevalence. Despite requiring some adjustments such as infrastructure modification to accommodate prawn migration, this investment in aquaculture also leads to an additional source of income and protein for farmers. The authors also proposed transforming removed vegetation in dams and nearby canals into compost for crop production, livestock feed or biofuel. They emphasise that through sound ecological design and management, dams can play an important role not only in alleviating poverty and food insecurity but also VBD transmission (Hopkins et al. 2021).
5 Barriers to overcome
It is clear from the examples of the consequences of agriculture on VBD ecology that although they are always unintended, these consequences have important and often negative impacts on human health, especially for poor and marginalised groups. With the necessity for a global agricultural scale-up to feed our ever-growing population, there is strong potential for these unintended side-effects of VBD transmission to increase alongside it (Rohr et al. 2019). The main barriers to solving this issue is a lack of problem ownership and a lack of intersectoral collaboration which leaves the agricultural and health sectors disjointed (Hawkes and Ruel 2006a).
The issue of problem ownership persists and is a barrier to efforts to tackle this issue. Traditionally, the health sector bears the burden of tackling problems relating to infectious disease transmission. On the other hand, development within the agricultural sector tends to focus on economic benefits to production and, more recently with Sustainable Intensification, on mitigating negative impacts on the environment. However, as we have highlighted, agriculture plays a role in VBD transmission, and it is crucial for the agricultural sector to take its fair share of responsibility for the health problems it creates (Lines et al. 2020).
There have been numerous calls over the past three decades (Hawkes and Ruel 2006b; Lines et al. 2020; WHO et al. 1996) for these sectors to align and begin to work together to overcome this ‘unavoidable’ and ‘unintentional’ issue, by acknowledging its existence and developing methods to avoid it. This, however, remains a daunting task (Hawkes and Ruel 2006b) which will require concerted collaborative efforts and resources from both sides. Researchers are often taught to work within their research silos and to disseminate their findings to like-minded researchers who have been trained in the same methods. As a result, it can be difficult to bridge disciplines and to find a common language between sectors. To tackle this issue of VBD transmission being driven by aspects of agricultural development we need innovation and strong will to facilitate interdisciplinary discussion, research and planning between the agriculture and health sectors, and indeed the water sector too. Such intersectoral collaboration can, however, often be held up by financial constraints. Generally, health sectors do not generate their own revenue, whereas agricultural sectors do.
One way in which the agricultural sector can be held accountable for their role in creating health risks is to share revenue with Ministries of Health and institutions focused on researching the links and possible solutions to this agriculture and VBD issue. An example of intersectoral research with resources provided by the agricultural sector is the CGIAR (agricultural organisation) funded Agriculture and Infectious Disease Group at the London School of Hygiene and Tropical Medicine (https://www.lshtm.ac.uk/research/centres-projects-groups/agriculture-infectious-disease-group). This is a multidisciplinary group involving infectious disease researchers collaborating with CGIAR centres such as International Livestock Research Institute (ILRI), the International Food Policy Research Institute (IFPRI), the International Institute for Tropical Agriculture (IITA), and Africa Rice Center. Their research is focused on the side-effects of agriculture on infectious disease with projects running on VBD, neglected zoonotic diseases and antimicrobial resistance.
Such collaborations create an ideal environment for the development of innovative co-benefits which include human health or vector-borne disease transmission as an outcome. It is important for experts from each sector to engage in dialogue on the issue and develop solutions which benefit them both. This will require robust research firstly into the cause-effect nature of agricultural impacts on VBD transmission and secondly into field-trials for innovative agricultural methods which can minimise this ‘cause’ from practices in the future. It is important for organisations within the agricultural sector to foot the bill of such research. Whilst they are conducting regular research on and developing agricultural practices that improve crop yield, it is important for them to consider the impact that these new practices may have on VBDs. Similarly, it is important for researchers within the health sector to be flexible and adapt their methods to fit within the framework of agricultural research, to ensure the smooth integration and bridging of agricultural and public health disciplines. This bridging of disciplines is not only required at the level of research communities, but also when it comes to funding: donor communities need to create more opportunities and prioritise these intersectoral issues.
Box 1: Priority actions for the health sector to overcome barriers and develop co-benefit solutions to agriculture-VBD issue
Develop capacity for dialogue and common research language with agricultural sector
Lead robust studies into the cause-effect of impacts of agriculture on VBD transmission
Adapt research methods to integrate within agricultural field trials
Box 2: Priority actions for the agricultural sector to overcome barriers and develop co-benefit solutions to agriculture-VBD issue
Develop capacity for dialogue and common research language with health sector
Provide expertise on agricultural research methodologies to facilitate integration of health research into trials
Fund agricultural research projects which prioritise health outcomes linked to vector-borne disease
6 Conclusions
In order to feed the world’s growing population, an increase in food production alongside policies to enhance food access are necessary. With expansion in agricultural development therefore an inevitable part of this strategy, it is imperative that the linked issue of agriculture increasing VBD transmission is acknowledged and tackled. It is clear that we need intersectoral work which bridges the two most involved disciplines of health and agriculture to begin to tackle this issue. This will involve disentangling the cause-effect relationships between the environmental drivers and VBD transmission, and facing issues such as the movement of vulnerable or infected populations. We need a co-benefits approach to find solutions which provide attractive outcomes for both sectors in order for them to be taken up and utilised as agriculture continues to develop. This will require concerted efforts by both sides to enable dialogue, sharing of resources and knowledge to develop innovative solutions, and to lead strong and robust research and field trials. We have seen that this is possible with the development and widespread uptake of Sustainable Intensification to mitigate agricultural impacts on the climate and the environment. This is promising and encourages the belief that agriculture can too be adapted to mitigate negative impacts on human health.
Acknowledgements
This work was partially funded by, and is a contribution to, the CGIAR Research Program on Agriculture for Nutrition and Health (A4NH). The opinions expressed here belong to the authors, and do not necessarily reflect those of A4NH or CGIAR. KC was supported by the Wellcome Trust’s Our Planet Our Health programme (grant number 216098/Z/19/Z), and IB was funded by the Bill and Melinda Gates Foundation (OPP# 1177272). We would like to thank the editors and reviewers for their feedback.
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