In early 2020, Harrison Hardy began his PhD on climate-adapted rice agricultural systems and was looking forward to various research trips to irrigated rice fields in Africa to research levels of malaria transmission. However, his travel plans were abruptly halted by the Covid-19 pandemic. He found himself restricted to a solitary UK laboratory where he made a surprising discovery about the effects of different types of organic manure on mosquito larvae. Harrison takes up the story.
Malaria is a huge problem in rice production areas due to the amount of standing water – it attracts mosquitoes to lay their eggs there. It's been known for a long time that rice cultivation leads to more mosquitoes, but it was disputed that it leads to more malaria.
My PhD project is looking at climate change adapted rice agricultural systems. It centres on a type of cultivation called the system of rice intensification – SRI - which was developed around 40 years ago in Madagascar to enhance yields whilst reducing agricultural inputs.
In the 1990s a series of experiments was carried out which culminated in a paper in 2001 that was dubbed the ‘paddies paradox’. It stated that although irrigated rice cultivation leads to an increase in the population of malaria vectors – i.e. more mosquitoes – it doesn’t necessarily translate into increased malaria transmission.
The reasons given for this were that the communities using irrigated rice cultivation systems as opposed to the traditional rain-fed systems, gained larger economic benefits. They had more money to buy mosquito nets for their beds and had access to preventative health care. They were better off health-wise than the non-irrigated rice growing communities, and this shielded them against the increased risk of transmission by isolating them from the higher mosquito abundances and allowing preventative and curative healthcare.
For a while this was a nice story that policy makers could use to bolster the argument that intensifying irrigated rice systems is good because it doesn’t lead to more malaria and it boosts the economy; it became a commonly held axiom. But starting my PhD, I read papers on communities living adjacent to a rice cultivation system across sub-Saharan Africa and I saw figures that pointed to increased malaria transmission. I wasn’t the only one who noticed, but there wasn’t a seminal paper.
In 2021 a colleague – Kallista Chan at the LSHTM (London School of Hygiene and Tropical Medicine) - published a meta-analysis re-examining this relationship and she discovered that prior to the early 2000’s, the ‘paddies paradox’ held true in that more mosquitoes didn’t necessarily mean more malaria, but that nowadays, that isn’t the case. More mosquitoes due to rice cultivation did lead to more malaria in adjacent communities.
One of the theories as to why this increase occurred, was that prior to the early 2000’s, rice-growing communities received mass distribution of insecticide treated bed nets, indoor residual spraying and malaria prophylaxes. But after the early 2000’s, when these mosquito counter measures were rolled out nationwide, continent-wide even, that relationship broke down.
If you’ve got an even spread of protection across communities with and without rice irrigation, but you’ve got more vectors in the irrigated areas, that translates into an increased transmission risk compared to the non-irrigated areas. However, this relationship is not well understood and requires further research.
In 2020, I was fascinated by the ‘paddies paradox’ and how SRI – system of rice intensification – might affect this supposed relationship, but as I couldn’t travel abroad to conduct any field research I had to radically rethink. I had access to a laboratory, I needed to stay within my remit of rice and mosquitoes – how could I do that in a lab?
I knew that within SRI one of the promoted practices is the use of organic fertilisers and I wondered how they might affect malarial mosquitoes? I managed to acquire some cow manure from Bore Place Farm in Kent, and I collected chicken droppings from a colleague’s hen coop. I brought these to the lab to see how the exposure to each type of manure when used as fertiliser affected the growing mosquito larvae. I took very young mosquito larvae, just 24 hours old, and transferred them into rearing trays with different concentrations of these manures. I raised them to adult as I measured different aspects of their life history traits.
The first thing I noticed was how the manure affected their survival; the larvae in the cow manure were fine, but many of those in the chicken manure died very quickly, especially at the higher concentrations. I also noticed how the two different species of mosquitoes I used, responded differently in unexpected ways. Compared to Anopheles gambiae s.s., Anopheles arabiensis seemed to be relatively tolerant to exposure to the lowest concentration of chicken manure, as their survival wasn’t impacted. Further, An. gambiae s.s. experienced greater development rates when exposed to cow manure whilst An. arabiensis did not. This may reflect differences in their underlying biology and ecology.
Later in the process, there was a clear difference in the number of adults produced under different treatment scenarios. The more
concentrated the chicken manure I used, the fewer adult mosquitoes there were. However, I saw that with both cow and chicken manure, the mosquitoes that did survive, grew into larger adults. Larger adults are generally considered ‘fitter’ as they tend to live for longer periods of time and reproduce more successfully.
Mosquito populations exposed to cow manure may therefore become larger in size and demonstrate a greater number of potentially infective bites, leading to increased malaria transmission. Although the adult mosquitoes that survived exposure to chicken manure were larger in size, there were fewer of them, so this might reduce the eventual transmission of malaria.
My research is still ongoing, and naturally I need to find out a lot more about any potential downsides of large quantities of chicken manure being introduced into the food chain and local water systems. I’m currently testing whether mosquitoes are averse to laying their eggs in water that contains cow, and/or chicken manure. There is a paper coming out on this soon.
After so long being stuck in a lab, I was delighted to get out to Tanzania in April 2022 to visit the rice field trials that I designed with a team based at Sokoine University of Agriculture who ran the trials in my absence. It was wonderful to finally meet the team in person and finally see my work in action!
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