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MAY 2020 GM Fungi to kill Mosquitoes Illegal experiments in Burkina Faso?

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Page 1: GM Fungi to kill Mosquitoes...kill mosquitoes were performed in the village of Soumousso in Burkina Faso in 2019. These were conducted in a tented facility, under a newly invented

PO Box 29170, Melville 2109, South Africawww.acbio.org.za

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GM Fungi to kill MosquitoesIllegal experiments in Burkina Faso?

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AFRICAN CENTRE FOR BIODIVERSITY – GM fungi to kill mosquitoes

ContentsOverview 3What is the genetically modified fungus? 5What was the experiment conducted in Soumousso, Burkina Faso? 5How ‘contained’ were these experiments? 6Safety concerns 8GM fungus as a successful malaria intervention tool? 9Conclusion 10References 11

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Acknowledgements

The ACB thanks Dr Eva Sirinathsinghji and Mariam Mayet for writing this research paper, and Lim Li Ching from Third World Network for contributing. We gratefully acknowledge the financial support of several donors. The views expressed in this publication are not necessarily those of our donors.

The African Centre for Biodiversity (ACB) is a research and advocacy organisation working towards food sovereignty and agroecology in Africa, with a focus on biosafety, seed systems and agricultural biodiversity. The organisation is committed to dismantling inequalities and resisting corporate-industrial expansion in Africa’s food and agriculture systems.

www.acbio.org.za

PO Box 29170, Melville 2109, Johannesburg, South Africa.Tel: +27 (0)11 486 1156

© The African Centre for Biodiversity

This publication is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License. This publication may be shared without modification for non-commercial use provided the African Centre for Biodiversity is acknowledged as the source. Prior written agreement is necessary for any commercial use of material or data derived from this publication.

Researched and written by Dr Eva Sirinathsinghji and Mariam Mayet, with contributions from Lim Li ChingProofing: Liz SpargLayout and cover: Adam Rumball, Sharkbuoys Designs

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Overview Conducted quietly and out of the public eye, a three-year experiment took place in Burkina Faso, to test the use of a genetically modified (GM) fungus to kill mosquitoes, on the pretext of developing malaria intervention tools. Although the experiment took place from 2015 to 2017, media announcements ‘notifying’ the citizenry of Burkina Faso were only made in May 2019, after the study was formally published in a US scientific journal1,2,3.

The experiment was conducted in the village of Soumousso, Burkina Faso by researchers based in the University of Maryland, United States, in collaboration with the Burkinabe Institut de Recherche en Sciences de la Santé/Centre Muraz, Bobo-Dioulasso. The published results describe the experiments as having exposed mosquitoes to GM fungi in enclosures surrounded solely by mosquito netting. The researchers have declared the technology as ‘close to field ready’’4 and that the GM fungus research and development ‘has progressed sufficiently for field application’5.

This project raises serious legal, biosafety, ethical, political and human rights concerns and questions regarding the conduct of the experiments. Serious doubts arise about the legality of the ‘semi-field’ experiments, as it

appears that the experiments do not satisfy the legal requirements for containment as is required by Law no 06402012 on the Safety Regime for Biotechnology (Burkina Faso’s Biosafety Law). If this is indeed the case, these dubious semi-field experiments would constitute an open release and should have triggered compliance with the public consultation and participation provisions of the Biosafety Law. Additionally, there were also a lack of, or any, meaningful public consultations prior to the commencement of the release, as is required by the law.

Astonishingly, approval was given for a ‘semi-field trial’. There is no mention of a ‘semi-field trial’ in the Burkina Faso Biosafety Law, as a legitimate activity that requires regulation. Indeed, there is no such concept in accepted biosafety parlance or regulation. This further calls into question the legality of the experiment and raises concerns regarding whether the approval is sound in law, as putative approval was given for what essentially constituted an unregulated activity. In any event, Article 17 of the Biosafety Law requires that a deliberate release of a genetically modified organism must be preceded by experiments where containment measures are first put in place for risk assessment and risk management purposes. Containment or contained use experiments thus constitute not only legal obligations for those carrying out laboratory and open field trials, but are also sound and well-established biosafety practices.

Experiments involving a new and potentially unsafe and risky genetically modified fungus to kill mosquitoes were performed in the village of Soumousso in Burkina Faso in 2019. These were conducted in a tented facility, under a newly invented category termed a ‘semi-field’ experiment. The invention of new, unscientific experimental categories sets a dangerous precedent that can bypass both national and international biosafety regulations and protocols regarding phased step-by-step robust biosafety testing. The process also lacks public participation.

The use of GM fungi to kill mosquitoes is being proposed by researchers to offer a quicker route to the market in a ‘new era of transgenic microbial control’. Indeed, the latest locust infestation in East Africa has prompted calls for the use of GM fungus14, with claims being made about the importation of non-GM and GM fungal biopesticides from China.

May 2020

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4The project also raises concerns in regard to the absence of testing done to ensure the safety of the GM fungus to people and the environment, thus preventing potential escape and persistence of GM fungi or infected mosquitoes from the experimental facility and providing sufficient safety protection for Burkinabe researchers who were exposed inside the experimental facility.

Wider concerns include misusing Burkina Faso as an experimental testing ground for new and controversial GM technologies. According to the researchers the project is ‘part of an international effort to advance the use of transgenic approaches for malaria control’4, conducted alongside other developments already underway. This includes the hugely controversial and contested Target Malaria project that aims to test extreme forms of GM ‘gene drive’ mosquitoes in Burkina Faso6,7. Indeed, some of the researchers are involved in both the GM fungus and Target Malaria’s gene drive projects.

As with gene drives, where public health interventions are being used to gain public and governmental acceptance for wider agricultural and US military funded gene drive technologies, it appears similar motivations are behind the GM fungus project. Indeed, the lead researcher of the project, Raymond St Leger, is developing entomological fungi for the agricultural industry8. Elsewhere he also states plainly that in order to convince regulators and carefully garner public acceptance for GM microbes such as this GM fungus, ‘clear and compelling impetus, such as the possibility of controlling vector-borne diseases’ is required, the latter which he also claims will ‘dominate the biopesticide market in the next 20–30 years’9. Suggestions to reduce persistence of fungal biopesticides as a way of increasing commercial sales are also indicative of the wider motivations of the developers.

St Leger has collaborated with Monsanto10, worked as a consultant for both private and public institutions, and in 2007 also served

on the policy-making board committee of the Bill Gates funded National Academies Committee ‘to study technologies to benefit sub-Saharan Africa and South Asia’11. St Leger also shares publications with academics12 who have undermined the United Nations Convention on Biodiversity (CBD), the place where international guidance and regulations on GMOs and new forms of genetic engineering including gene drives are adopted. Through freedom of information legal requests, the academics were recently exposed to have convened meetings with the industry lobby groups representing Monsanto, Cargill and others13.

While gene drive technologies are still in the development phase, the use of GM fungi to kill mosquitoes is being proposed by researchers to offer a quicker route to the market, which can be deployed in the meantime. Gene drive technologies are suffering from technical obstacles and difficulties, as well as regulatory barriers due to the unprecedented biosafety and ethical concerns and challenges they raise. This species of fungus is easy to genetically modify, cost-effective to produce on an industrial scale, and can be regulated under already existing biosafety regulations in Burkina Faso. It is thus being suggested as a more immediate tool to be released under a ‘new era of transgenic microbial control’5.

Many insects are also currently recalcitrant to genetic engineering techniques, thus paratransgenesis – the genetic engineering of one species (usually a microorganism) to exert desired effects in/on a host – provides an alternative means to ‘modify’ mosquitoes and other insect species. Indeed, the latest locust infestation in East Africa has prompted calls for the use of GM fungus14, with a Chinese media report also claiming the importation of non-GM and GM fungal biopesticides from China15, although this remains to be verified. Other paratransgenesis approaches are also underway, such as vector control strategies, where GM bacteria are deployed to secrete anti-malaria parasite proteins16.

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What is the genetically modified fungus? The GM fungus is called Metarhizium pingshaense, a type of parasitic fungus that infects insects, termed entemopathogenic fungi. They live in the soil in the vicinity of plant roots, called the rhizosphere, where it is suggested they interact with plants in a mutually-beneficial symbiotic relationship by promoting plant growth (by producing plant hormones)15, as well as inside infected insects. To reproduce, the fungus infects insects by directly penetrating the cuticle with its spores, where it colonises the body and causes paralysis, killing the insect in the process. The fungus then emerges from the dead body to produce more spores.

Metarhizium species have already been tested as bio-pesticides for malaria vector control, but researchers have claimed that they are not effective in killing mosquitoes quickly enough to reduce malaria spread. Non-genetically modified Metarhizium species have also been tested in other African countries (South Africa, Sudan, Zambia, Mozambique, Tanzania) for agricultural pests with varying success in reducing populations14. The researchers claim that by using genetic engineering they can increase the efficiency of the fungus to

kill mosquitoes, and thus reduce mosquito numbers and thence malaria transmission.

The GM fungus was developed by introducing a toxin from the lethal Australian Blue Mountains funnel-web spider (Hadronyche versuta), called ω/κ-hexatoxin-Hv1a, referred to as ‘Hybrid’, into the M. pingshaense fungus. The researchers claim that while the venom of this spider can be lethal to humans, the toxin that they have isolated from the venom is only lethal to insects. However, as discussed below, experiments and thus data are lacking to substantiate safety claims to either human or other non-target organisms.

What was the experiment conducted in Soumousso, Burkina Faso? To test the effects of the GM fungus on mosquito survival, researchers released (non-GM) local mosquitoes inside a tented facility, ‘MosquitoSphere’, erected next to the village of Soumousso, Burkina Faso. Satellite images of the facility show that it is located close to residential housing. This tent consists of a greenhouse frame, covered with mosquito netting. The researchers refer to this experiment as a semi-field

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6trial, where the mosquitoes are exposed to environmental conditions such as sunlight and rainfall. Inside the MosquitoSphere, there are numerous experimental ‘huts’, designed to mimic an African house. Inside these ‘huts’ the researchers placed cotton sheets covered with the GM fungus, as well as carcases of calves and sugar meals for the mosquitoes to feed on.

A series of experiments were conducted. Initial experiments were performed to see how many mosquitoes could be infected with the GM fungus. For this, 100 Anopheles colluzzii mosquitoes were released at dusk, and mosquitoes were collected in the morning and tested for GM fungal infection. This experiment was repeated seven times during 2015.

The main experiment assessed the effects of GM fungal infection in reducing Anopheles colluzzii mosquito populations over several generations. This involved the release of one thousand males and five hundred female mosquitoes, with population and egg numbers and larvae breeding sites recorded over a period of up to nine weeks. This experiment was repeated three times during the rainy season in 2017.

How ‘contained’ were these experiments? The proclaimed rationale for the experiments was to expose the mosquitoes to environmental conditions. As such, the MosquitoSphere containment measures appear to have consisted of mosquito netting surrounding a metal greenhouse frame. The publication describes the experiments in a variety of ways, including ‘semi-field trial’, ‘contained field trial’, and ‘contained, semi-field trail’. The researchers appear to have obtained authorisation for both ‘semi-field’ and ‘lab’ work. However, it appears that such definitions/concepts are not included in the Burkinabe Biosafety Law, which only includes regulation for containment or environmental releases. Of utmost concern is whether the developers may have gained approval for an unregulated activity.

If, indeed, the experiments were approved as containment/‘contained use’ experiments, then it appears as if they flouted the required containment measures for the GM fungus. The Burkinabe Biosafety Law defines containment in Article 7 as ‘isolation of genetically modified organisms with a view to limiting actually the contact with the external environment and the impact on this environment’.

Indeed, while it is the fungus that is genetically modified and thus subject to regulation, the measures implemented by the developers focus on the mosquito, that is, the mosquito net. No information on containment measures in relation to the GM fungus, to prevent escape at entrances/exits, such as the use of double-doors, disinfectant or protective clothing were presented.

Additionally, the fungus is a pathogen to insects, which means that the biosafety norms for contained use that apply to pathogens should also apply to this GM fungus. However, there is no mention of what biosafety level approval was sought and granted, as is required by the Biosafety Law. Even regarding mosquito escape, there is no mention of whether the netting used meets arthropod containment standards.

This calls into question whether the mosquito netting was adequate to prevent escape of GM fungal spores. Potential for damage to the netting by rain, wind and storms, for example, may also have provided a potential escape route. Researchers’ descriptions of limited escape, due to the stickiness of the fungal spores and susceptibility to degradation following sun exposure, are merely assumptions. These factors may not be sufficient to prevent escape and survival in the open environment. Media coverage shows images of researchers working inside the MosquitoSphere in what appears to be normal clothing16 (no protective or laboratory clothing was pictured, for example, laboratory coats, masks, booties, hairnets and so forth), allowing potential contamination of clothing with the fungal spores, which may then be carried outside the facility and into public spaces. Such shocking lax and unscientific procedures also risk exposing the Burkinabe researchers to the GM fungus.

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There is no mention of any monitoring outside the facility for unintended escape of either infected mosquitoes, or the GM fungus itself as is required by various provisions of the Biosafety Law, including for example, Articles 28, 35 and 44. Once outside the facility, there is potential for GM fungal persistence. Because this fungal species reproduces by infecting mosquitoes, any escape of either GM fungal spores or by an infected mosquito means this could lead to GM fungal reproduction and persistence in the wild. The researchers claim that managing any spread of GM fungus would be easier than managing the spread of a GM mosquito, as many dead mosquitoes are scavenged, which would prevent any establishment in the environment4. However, such unfounded assumptions should not supplant responsibility on the part of those conducting the project to put in place safety and precautionary measures to prevent unwanted/unintended spread. It is highly questionable that the containment measures described by the researchers during 2015–17 meet biosafety ‘contained use’ standards and should more accurately be regarded as an ‘environmental release’. Yet no registration under the UN Biodiversity Conventions registry, the Biosafety Clearing House has been made, as required under the Cartagena Biosafety Protocol, to which Burkina Faso is a Party.

Article 39 of the Burkinabe Biosafety Law creates a mandatory obligation for public consultations prior to approval being granted for release of any GMO into the environment. The processes described by the research publication for obtaining consent from community residents for these experiments were that ‘village leaders in Soumousso and local government representatives were consulted with and approved the proposed activity’4. Unfortunately, this public consultation seems to be merely a top-down box-ticking exercise to garner ethics approval. In reality it keeps the communities invisible and excluded from an experiment that directly affects them. The lack of public notification and participation prior to environmental release would render the experiments illegal.

Adherence to a progressive approach that first includes contained use experiments between laboratory and field experiments is essential biosafety practice. Failure to do so violates fundamental principles of sound and good biosafety practice and is not consistent with the spirit, intention, objectives and provisions of the Biosafety Protocol, or, for that matter, the Burkinabe Biosafety Law.

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Safety concerns These experiments present numerous biosafety concerns for both people and the environment, which call into question the claims of safety presented by the researchers.

First, the claims of safety of the ‘Hybrid’ toxin inserted into the GM fungus do not appear to be supported by available scientific literature. The researchers state that Hybrid toxin is only active in insects. However, the literature they cite to substantiate their claim is based on a related, but different toxin. While the cited toxin acts to block a type of sodium channel in neuronal cells, the Hybrid toxin blocks potassium and calcium channels. Data assessing human toxicity of the Hybrid toxin is lacking. Instead it appears as if claims of safety have been assumed, based on how the scientists think the toxin’s mechanism of toxicity functions, and assumes that there is no other way in which the toxin could exert toxicity. This goes against basic scientific principles, which demand that scientific claims should be substantiated by empirical

evidence. It also violates the precautionary approach that aims to ensure the safety of human health in the event of exposure to any GMO that may cause adverse effects.

The recent approval by the US Environmental Protection Agency (US EPA) of the Hybrid toxin as a biopesticide is also cited to bolster safety claims. However, the US EPA describes the toxin as a ‘moderate skin and eye irritant’17. It is pertinent to note that this toxicity appears to exert a completely different mechanism to the toxin that kills mosquitoes. The EPA further states that this toxic effect can be mitigated by wearing protective clothing. (Any open field trial release would expose people without protective clothing to the GM fungus). The US EPA also waived requirement for sub-chronic, chronic, developmental, reproductive toxicity, genotoxicity and oncogenicity studies, making its approval entirely inadequate as proof of safety. Suggestions to combine the GM fungus with chemical pesticides add to the complexity of the biosafety concerns, with potential interactions or synergistic effects on toxicity, which raises an added concern.

Credit: Hector Conesa / Shutterstock.com

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9With the transgene being made synthetically, and taking into account the lack of detailed information on the exact genetic sequences that were inserted into the GM fungus, it remains unknown if the sequence is indeed identical to the naturally existing spider toxin. Without a single toxicology test presented on the GM fungus itself, it is also impossible to rule out whether the genetic engineering process has altered the properties of the toxin or the fungus. This may alter the GM fungi’s toxicity to humans and other non-target organisms; or affect mosquitoes in unintended ways. Unintended effects were, indeed, documented in infected mosquitoes, who laid eggs significantly earlier than uninfected mosquitoes and those infected with the non-GM fungus.

The researchers have only tested toxicity of the GM fungus on a few species of non-target insects, claiming lack of toxicity to locusts and honeybees, despite not presenting the data on locusts. However, a separate paper has been published using the same Hybrid toxin introduced into another GM fungal species, which shows that the toxin is able to kill locusts18. Claims of safety to non-target organisms such as beneficial insects have also been made, based on the specificity of the M. pingshaense species to infect a very limited number of insect species. Concerns remain, however, of gene flow from this species to another that may have a different target host range and thus infect different non-target species.

Another claim made is that human or non-target organism exposure would be limited, as the transgenic toxin is only produced inside the fungus upon infection of an insect. However, data to prove a lack of expression in the fungal spores under various conditions is lacking.

Natural, non-GM Metarhizium fungal species have also been associated with serious adverse health effects in humans, including rare cases of death following infection by the fungus, especially people whose immune system is compromised19. A weak immune system can result from numerous circumstances, including malnutrition, immune diseases, or cancers, for example. Insufficient data on M. pingshaense raises concerns that similar effects may well occur

with this species, where increased exposure on bed nets following an open environmental release would be likely.

Finally, no tests appear to have been published to assess whether the GM fungus would alter the relationship with plant roots, and thus affect plants differently. Metarhizium fungal species are abundant in the rhizosphere – the soil surrounding plant roots that is occupied by microorganisms associated with the plant, known as the root microbiome. If, as hypothesised by the researchers themselves20, M. pingshaense forms beneficial relationships with plant roots that promote plant growth, then it becomes imperative that tests are done to ensure that the GM fungus does not adversely affect soil and plant health, with knock-on effects on the wider ecosystems and farmers’ livelihoods.

GM fungus as a successful malaria intervention tool? While experiments showed a reduction in mosquito numbers and reproduction rates following exposure to the GM fungus (as well as non-GM fungus) across (only) two generations, questions still arise as to its appropriateness as a successful malaria intervention tool.

Reduction in numbers was variable depending on the weather, with increased inconsistency in those experiments that took place approaching the dry season and thus more similar to the outcomes observed with the non-GM fungus. Data numbers were only given for the more successful replicates of the study, however, so direct comparisons cannot be made between those that were more successful and those that were not.

Further, while the main research publication present results with only A. coluzzii mosquitoes, the supplementary data also shows some results of experiments conducted with A. gambiae. The reason for excluding this data or any mention of A. gambiae experiments in the main publication is not declared, raising questions regarding

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10efficacy against the main malaria-carrying mosquito in Burkina Faso. Effects across the generations of A. gambiae should also be presented if this technology can be claimed as offering promise in tackling malaria in the real world. Indeed, the supplementary results for initial experiments showed that survival of A. gambiae following exposure to freshly applied GM fungus was not decreased in comparison to the non-GM counterpart. Only exposure to three- to seven-week old GM fungus reduced A. gambiae mosquito survival more effectively than the non-GM counterpart. Even for A. coluzzii, the only clear improvement in the two-generation experiment was reduced A. coluzzii mosquito survival after exposure to the four- to seven-week old GM fungus, showing that its toxicity lasts longer than the non-GM fungus. How this would translate to mosquito population reduction in the wild remains dubious.

Overall, these results do little to illustrate the potential of this approach as a sustainable, effective malaria intervention tool. Indeed, the researchers themselves claim that resistance to the GM fungi may well occur, and to counter this, it may be necessary to have multiple virulence-enhancing genes in the same fungus or to deploy several species each utilizing different toxins with different modes of action for both increased toxicity and resistance management. Yet again, the reality of a GM approach, as experienced to date with GM crop cultivation, is at best, a short-term solution that locks farmers, and now potentially public health programmes into a never-ending GM/chemical product cycle.

As previously highlighted7, reductionist, biomedical malaria public health programmes that focus solely on mosquito vector control and not wider social determinants of malaria, a complex disease, have only worked in particular contexts and more so where social determinants of disease

are also addressed – for example, countries where wider healthcare infrastructure was in place, where economic circumstances are sufficient to reduce exposure and cover costs of existing treatments, and/or where environmental or agricultural programmes have been conducive to mosquito control. Indeed, numerous countries have recently been successful in eradicating malaria (Paraguay, Sri Lanka, Algeria and Argentina), or significantly reducing it (Mayanmar), in large part due to improvements in healthcare infrastructure that have increased diagnostics, treatment and surveillance in addition to other integrated approaches.

As the COVID-19 pandemic has cruelly highlighted, a focus on yet-to-be developed technological solutions in nations such as the UK has been extremely costly in directing emphasis away from existing measures that have thus far been more successful in staving off losses of life in many nations, including in Africa, the Caribbean and Asian countries.

Conclusion Claims that the technology is ‘close to field ready’ suggest that developers may be expecting to progress to open trials in the near future. Written requests (sent in 2019) to the researchers for information on when such open field trials are expected did not receive any response. The lack of transparency fuels mistrust in researchers who have links to agricultural or biotechnology corporations in pursuit of commercial agricultural biopesticide sales.

Biosafety laws, health and environmental safety and human rights must be respected; public participation mechanisms must be followed, and the public at large given genuine opportunities to have their voices heard.

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References 1. “Burkina Faso research may prove a malaria breakthrough”, Africa Times, 31 May 2019, accessed 6 August 2019.2. “GM fungus rapidly kills 99% of malaria mosquitoes, study suggests”, BBC News, 31 May 2019, accessed 6 August

2019.3. “Fungus modified with spider venom offers new hope in fight against malaria”, CNN health, 31 May 2019, accessed 6

August 2019.4. Lovett B, Bilgo E, Millogo S, Ouattarra A, Sare I, Gnambani E, Dabire R, Diabate A, St Leger RJ (2019) Transgenic

Metarhizium rapidly kills mosquitoes in a malaria-endemic region of Burkina Faso. Science 364(6443):894–897.5. Lovett B, Bilgo E, Diabete A, St Leger RJ (2019) A review of progress toward field application of transgenic

mosquitocidal entomopathogenic fungi. Pest Manag Sci 75(9): 2316-2324. doi: 10.1002/ps.5385.6. ACB (2019) Gene drives organisms: What Africa should know about actors, motives and threats to biodiversity and food

systems. African Centre for Biodiversity, Johannesburg. https://acbio.org.za/en/gene-drive-organisms-what-africa-should-know-about-actors-motives-and-threats-biodiversity-and-food.

7. ACB (2018) AU’s premature and misguided endorsement of controversial, unproven gene drive mosquitos for malaria ‘eradication’ in Africa. African Centre for Biodiversity, Johannesburg. https://acbio.org.za/en/aus-premature-and-misguided-endorsement-controversial-unproven-gene-drive-mosquitos-malaria.

8. Raymond John St. Leger. Department of Entomology, University of Maryland https://entomology.umd.edu/st-leger-raymond-j.html, accessed 31 July 2019.

9. Lovett B and St Leger R (2018) Genetically engineering better fungal biopesticides. Pest Manag Sci, 74(4):781–789. doi:10.1002/ps.4734.

10. Freimoser FM, Screen S, Screen S, Hu G, St Leger R (2003) EST analysis of genes expressed by the zygomycete pathogen Conidiobolus coronatus during growth on insect cuticle. Microbiology 149(Pt 7):1893–1900.

11. ‘Raymond St Leger’, Wikipedia. https://en.wikipedia.org/wiki/Raymond_St._Leger, accessed 31 July 2019.12. Hokanson KE, Dawson WO, Handler AM, Schetelig MF, St Leger RJ (2014) Not all GMOs are crop plants: Non-plant

GMO applications in agriculture. Transgenic Res 23(6):1057–1068.13 Corporate Europe Observatory (2018) Biosafety in Danger. How industry, researchers and negotiators collaborate

to undermine the UN Biodiversity Convention. https://corporateeurope.org/en/food-and-agriculture/2018/06/biosafety-danger.

14. Alliance for Science (2020) Scientists call for innovation in fight against destructive locust pests. https://allianceforscience.cornell.edu/blog/2020/02/scientists-call-for-innovation-in-fight-against-destructive-locust-pests/, accessed10 May 2020.

15. China’s green zombie fungus could hold key to fighting East Africa’s swarms of locusts. South China Morning Post, 22 February 2020. https://www.scmp.com/news/china/science/article/3051819/chinas-green-zombie-fungus-could-hold-key-fighting-east-africas, accessed 18th May 2020.

16. ACB (2020, forthcoming) Profiteering from health and ecological crises in Africa: The Target Malaria project and new risky GE technologies. African Centre for Biodiversity, Johannesburg.

17. De Faria MR and Wraight SP (2007) Mycoinsecticides and mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43(3):237–256.

18. Nishi O and Sato H (2019) Isolation of Metarhizium spp. from rhizosphere soils of wild plants reflects fungal diversity in soil but not plant specificity. Mycology 10(1): 22–31.

19. “Inside Burkina Faso’s mosquito dome, where venomous fungus is put to the test”. Atlas Obscura, 14 June 2019. https://www.atlasobscura.com/articles/venomous-fungus-mosquito-dome, accessed 31 July 2019.

20. New York State Department of Environmental Conservation (2016) Registration of the new active ingredient GS-omega/kappa-Hxtx-Hv1a contained in the pesticide products Spear and Spear T. http://pmep.cce.cornell.edu/profiles/biopest-biocont/bioinsect/gs-omega_kappa-hxtx-hv1a/gs-omega_kappa-hxtx-hv1a_reg_1216.pdf.

21. Fang W, S-L Lu, King GF, St Leger RJ (2014) Construction of a hypervirulent and specific mycoinsecticide for locust control. Scientific Reports 4:7345.

22. Brunner-Mendoza C, Reyes-Montes M, Moonjely S, Bidochka MJ, Toriello C. (2018) A review on the genus Metarhizium as an entomopathogenic microbial biocontrol agent with emphasis on its use and utility in Mexico. Biocontrol Sci & Tech 29(1):83–102. doi: 10.1080/09583157.2018.1531111.

23. Liao X, Lovett B, Fang W, St Leger RJ (2017) Metarhizium robertsii produces indole-3-acetic acid, which promotes root growth in Arabidopsis and enhances virulence to insects. Microbiology 163(7):980–991. doi: 10.1099/mic.0.000494. Epub 2017 Jul 21. PMID: 28708056.

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