Towards Understanding And Management Of Vector-borne Plant Virus Impacts On Nutrition In A Changing Climate

Vector-borne plant viruses and the diseases they cause (plant VBDs) provide a functional link between climate and human health. Weather and climate both impact insect vector populations over short and longer-term timeframes, affecting plant VBD prevalence and severity. Climate change alters the distribution and abundance of plant disease vectors, including important agricultural pests such as whiteflies and aphids by influencing their phenology, migration, number of generations per year and overwintering strategies (Aregbesola et al, 2019; Tougeron et al, 2018). Both whiteflies and aphids have world-wide distributions and comprise multiple species that are morphologically difficult to distinguish. Each transmit a multitude of plant viruses that devastate crop yields at a global scale and exhibit resistance to pesticides (Troczka et al 2021). The impacts of climatic factors on plant pest performance is complex and variable (e.g. Beetge and Krüger, 2019) and therefore difficult to predict: temperature plays a key role and this can be influenced by humidity, rainfall/water stress, and wind patterns. Ecoclimatic modelling of B. tabaci shows that increasing temperature and reducing rainfall were key to increased climatic suitability and this correlated with increased prevalence of both B. tabaci and crop diseases spread by B. tabaci (Kriticos et al, 2020). Emergence of new plant diseases or significant shifts in distributions can shock agricultural productivity and lead to displacement where livelihoods are lost causing hunger and poverty (Risatino et al, 2021).

Plant VBDs reduce usable yields of a range of nutritionally important crops (particularly fruit, vegetables, legumes, nuts, seeds) which restricts dietary diversity, and can lead to micronutrient deficiencies. Additionally, future environmental changes are predicted to reduce yields of fruit, nuts and seeds (Alae-Carew et al, 2020). Malnutrition from poor diets can impact human immunity to and resilience against communicable diseases (including human and zoonotic VBDs; Muurlink and Taylor-Robinson, 2020) and is now the leading driver of non-communicable diseases worldwide: 2 billion people worldwide suffer from deficiencies of important micronutrients including vitamin A, iron and zinc (see HCN Briefing 1, 2021). Pesticides used to control insect vectors of plant viruses can have detrimental effects on human, animal and ecosystem health. Recent pesticide bans in Europe have led to increases/resurgences in plant VBDs. Integrated pest management (IPM) has been shown to have multiple beneficial impacts in Africa: increased crop yields and increased income for farmers, lower pesticide applications quantities and lower levels of pesticide toxicity leading to reduced environmental and human health impacts (Midingoyi et al, 2019). Climate-smart pest management offers an improved approach that considers climate projections alongside pest surveillance, detection, management and advice to farmers, pest risk forecasting, and the wider enabling policy, regulatory and funding environment (Heeb et al, 2019). However, it is unclear in regions such as Africa what climate services are available, used, needed, or preferred by end-users (including agricultural extension officers and plant health quarantine officers) to augment IPM-type approaches towards being climate-smart.

Reacting to these challenges and opportunities requires an interdisciplinary approach which considers interconnections between plants and insect vectors within a changing climate, and how these affect end-users. This topic presents an exciting opportunity to bridge these disciplines and build a work area that could, in the longer term, contribute to efforts for food and nutrition security alongside promoting nutritional sustainability and climate change adaptation and resilience.

This project will take forward actions which emerged from an Elizabeth Blackwell Institute-funded international and interdisciplinary workshop held in July 2022. The workshop brought together researchers and experts from the UK, Kenya, and USA to identify the most interesting and pressing research priorities within the space of plant-related vector-borne diseases, human health and climate. Workshop participants represented a diverse range of disciplines including detection and diagnosis of plant VBDs and insect vectors, capacity building, disease control, climate, nutrition and health. It was clear during the workshop that more time was needed to allow better understanding of key terms, concepts and methods. Discussions from the workshop gave rise to three linked research areas to explore. Briefly, these were (1) a ‘top 3’ list of nutritionally (and culturally) important crop types severely impacted by plant VBDs; (2) the role of different whitefly-vectored and aphid-vectored viruses in reducing nutritionally important crop yields globally, and the increase in prevalence of these viruses and their insect vectors in vulnerable regions over the last ~30 years (considering the impact of agricultural intensification and climate on emergence, selection pressures and disease resistance); and (3) identification of broadly applicable integrated (and climate smart) pest management approaches for the sustainable management of leading vectors of disease.

In this project, the PI (Dr Nina Ockendon-Powell) will work with Co-Investigators Prof. Dan Bernie (MOAP Fellow, Climate and Health Sciences), Dr Eunice Lo (University of Bristol Research Fellow in Climate Change and Health), and Dr Angeliki Papadaki (University of Bristol Senior Lecturer in Nutrition) to:
1. Conduct a dataset gathering exercise as a means to (1) develop a catalogue of plant VBD, climate, and nutrition/health datasets from Africa, UK and Europe for mining in preparation for larger grant applications and (2) developing a better shared understanding of key terms, concepts and methods to refine research questions concerning how climate affects plant VBDs, and how such changes are leading to human health impacts. Using papers identified by a recent plant VBD landscape review commissioned by the CONNECTED Network, source and collate most up-to-date datasets of plant VBD distribution, yield loss and climate impacts for nutritionally relevant crops. Identify most appropriate and accessible weather, season and climate projection data for considering questions relating to plant VBD emergence, spread, severity, and management. Identify publicly available and/or systematically collected community-level nutrition/health datasets. Datasets to be used in future systematic reviews/meta-analyses. [NOP, DB, EL]
2. Link with current related UoB projects integrating climate and health (e.g. Micro-Poll, Prof Jane Memmott): develop a better understanding of methods which are transferable to this project and forge new academic links with related specialists. [NOP, DB, EL]
Objectives 1 and 2 will enable the development of a roadmap for climate-plant VBD-health research which will be pursued in further funding applications.
3. Supplement recent plant VBD landscape review with additional evidence concerning selected virus (co-)infection, plant-virus-vector interactions, and broadly applicable sustainable management options with independent plant virologist/plant disease epidemiologist Dr Lawrence Kenyon. Develop outline draft of article for publication. [NOP]
4. Lead a systematic review of what constitutes the African traditional diet to begin identifying whether plant VBDs are impacting adherence to the traditional diet, considering the role of the nutritionally (and culturally) important crops outlined above. Develop an outline draft of article for publication. Focusing on traditional diets is of high relevance to environmental discovery because they reflect cultural, culinary and agricultural traditions and they are plant-based with few animal products. As such, they promote dietary diversity and beneficial health outcomes, and are also environmentally-friendly as they utilise reduced land, water and energy, focus on seasonal and local foods and are linked to reduced pollution (Burlingame, 2012; Jones et al, 2016). [NOP, AP]

Additionally, this project will support the running of an in-person workshop in East Africa to capture a qualitative dataset from end-users (extension and quarantine officer) on existing, utilised, and preferred climate services for pest and disease management, considering short-term (weather/season) and longer-term (climate projections) perspectives. The workshop will be organised and run by the CABI Plantwise Plus programme. The findings from this workshop will complement current research with UoB MOAP Fellow Dr Joseph Daron and University of Exeter/Met Office (Dr Catherine Bradshaw and Dr Debbie Hemming) being funded by the CONNECTED Network UKRI impact realisation grant.