A prioritisation study was conducted to address the lack of adequate information about potential pests likely to be introduced in Zambia and become invasive. The study was conducted by subject matter experts from relevant institutions in and outside Zambia. Although this study focused on major pest categories, this paper only addresses bacteria and Protista. A list of 306 bacterial and 10 Protista species adjudged to affect plants was generated using CABI’s Horizon Scanning Tool. The 316 (total) pest species were refined to focus on pests that affect value chains important to Zambia’s economy. This resulted in a final list of 133 bacteria and eight Protista. Four additional bacteria species considered of phytosanitary interest were added and all 137 bacteria and eight Protista species were subjected to a rapid risk assessment using agreed guidelines. Vectors reported to transmit any of the pathogenic organisms were also subjected to a risk assessment. A proportion of 53% (n = 77 of 145) comprising 73 bacteria and four Protista species were reported as present in Africa. Of these, 42 (57%, n = 73) bacterial species and two (n=4) Protista species were reported in neighbouring countries. Considering a cut-off of 54, the highest scoring pests were 40 bacteria (highest score of 140) and three Protista (highest score of 125). Three actions were suggested for high-scoring pests, a detection surveillance, a pest-initiated pest risk analysis (PRA) or a detection surveillance followed by pest-initiated PRA. A “no action” was suggested where the risk was very low although, for some pathogenic organisms, a “no action” was followed by periodic monitoring. This information will contribute towards proactive prevention and management of biological invasions.

Horizon scanning, invasive alien species, pest prioritisation, pest risk, risk assessment

A number of alien species ¹ have been introduced in sub-Saharan Africa (SSA) in the last couple of years through intentional or unintentional human-mediated activities (Faulkner et al. 2020; Uyi et al. 2021; Mulema et al. 2022). The majority of these aliens have become invasive ² (here referred to as invasive alien species or IAS) as evidenced by their effects on agricultural productivity, human health, livelihoods and biological diversity (Early et al. 2016; Paini et al. 2016; Pratt et al. 2017). In phytosanitary terms, such organisms are considered pests ³ and classified as quarantine ⁴ pests if not yet widespread within a target region. The primary objective of National Plant Protection Organisations (NPPOs) is to prevent the introduction and spread of quarantine pests through regulation. The effect of IAS on agricultural productivity is characterised with loss of income due to reduced crop yields, compromised quality of harvested produce and increased management costs (Eschen et al. 2021).

For instance, Eschen et al. (2021) estimated losses associated with the invasive lepidopteran insect, Spodoptera frugiperda in SSA at USD 9.4 Bn annually. It has also been estimated that the invasive plant pathogenic bacterium, Xylella fastidiosa, will cause losses ranging from USD 1.9 to USD 5.2 Bn if no corrective measures, such as deploying resistant cultivars and application of appropriate phytosanitary measures ⁵, are implemented (Schneider et al. 2020). Such phytosanitary measures include control of vectors that transmit the bacterium, suppression of inoculum and removal of infected host plants (Almeida et al. 2005; Liccardo et al. 2020; Castro et al. 2021; Quetglas et al. 2022). In SSA, management of IAS is associated with extensive indiscriminate application of mostly hazardous inorganic pesticides due to limited cost-effective and efficient pest control options (Siddiqui et al. 2023). This has resulted in the production of unsafe food and feed for human and animal consumption and reduced biodiversity due to the adverse effects of hazardous agro-chemicals on non-target species (Martinez et al. 2020).

The most cost-effective, efficient, sustainable and practical management option for IAS is through restricting entry or enabling early detection in case of entry, followed by prompt mitigation of pest spread and associated adverse effects of the IAS. However, this requires availability of adequate and up-to-date information about potential invasions (Mulema et al. 2022). Horizon scanning is one approach through which such information can be generated and availed to risk managers, policy and decision-makers (Sutherland et al. 2010, 2020; Matthews et al. 2017). It is the systematic search for potential biological invasions and an assessment of their potential impacts on the economy, society and environment considering possible opportunities for mitigating the impacts (Sutherland et al. 2008, 2010, 2020; Roy et al. 2014). Information generated from horizon scanning can be used to support planning on management of IAS at country and regional level and provide information for policy and practice (Caffrey et al. 2014).

At country level, horizon scanning has been used to prioritise IAS in countries, such as Cyprus (Peyton et al. 2019), Spain (Gassó et al. 2009; Bayón and Vilà 2019), United Kingdom (Sutherland et al. 2008), see also Great Britain (Roy et al. 2014) and recently in Ghana and Kenya (Kenis et al. 2022; Mulema et al. 2022). At the regional level, horizon scanning has been utilised in the European Union (Roy et al. 2019), Central Europe (Weber and Gut 2004) and Western Europe (Gallardo et al. 2016). CABI is also considering assessing at regional level, the risk of new IAS to the Regional Economic Blocks of the East African Community (EAC), Economic Community of West African States (ECOWAS) and Southern African Development Community (SADC). There is a paucity of information on potential biological invasions in most SSA countries resulting in reduced capacity for timely detection, mitigation and management of pertinent pest threats in the region. Therefore, the current study applies the horizon-scanning approach to generate useful pest-related information for Zambia that will enhance timely action on IAS. The study was conducted with the ultimate objective of prioritising pests that are not currently recorded as present in Zambia, but could be introduced and become invasive in future, thereby threatening the economy by negatively impacting on agriculture, biodiversity and forestry.

The full horizon-scanning assessment covered plant pests in the categories, Arthropoda, Bacteria, Chromista, Fungi, Mollusca, Nematoda, Protista, Viruses and Viroids. Previously, lists of candidate IAS for risk assessment were generated by experts through extensive literature searches (Weber and Gut 2004; Sutherland et al. 2008; Gassó et al. 2009; Roy et al. 2014; Gallardo et al. 2016; Bayón and Vilà 2019); however, CABI has developed a Horizon Scanning Tool to support identification of pests for risk assessment. The Horizon Scanning Tool was previously applied in studies conducted in Kenya in 2018 (Mulema et al. 2022) and Ghana in 2020 (Kenis et al. 2022). The tool can be accessed directly from https://www.cabi.org/HorizonScanningTool and via the CABI Compendium (https://www.cabidigitallibrary.org/cabicompendium).

The initial search yielded a total of 306 plant pathogenic bacteria and 10 protists. However, following a cleaning process to remove pests represented only by genus names, the list was narrowed down to 283 bacterial and 10 Protista species that were eligible for assessment (Suppl. material 2). The cleaned list comprised of 43 species reported as invasive, all of which were bacterial species. The list was further refined to focus on pests that damage value chains relevant to Zambia which resulted in a list of 137 bacteria (Suppl. material 3) and eight Protista (Suppl. material 4) species resulting in a total of 145 pests. It is this list that was subjected to rapid risk assessment using the guidelines presented in Suppl. material 1, but also briefly described in the methodology.

In addition, species, not yet reported as present in Zambia, but adjudged to be of phytosanitary concern, were added to each respective pest category although this was only possible for the bacterial species. The additional pests are highlighted in the column named “From horizon scanning” (Suppl. materials 3, 4) particularly those indicated as “N” (for NO) in the list, denoting that the given pest was not part of the original scanning process. Vectors that have been reported to transmit the assessed pest species, especially for the bacteria species were also assessed to establish their associated level of risk (Suppl. material 5). For both categories (Bacteria and Protista), 53% (n = 77 of 145) were reported in Africa. Of the 53% reported in Africa, 60% (n = 46 of 77) were reported for neighbouring countries to Zambia (Suppl. materials 3, 4). Such pests had very high overall risk scores because of their increased likelihood of entry.

Horizon scanning was utilised to select pest species not yet reported as present in the region at risk (Zambia) followed by an assessment of their likelihood of introduction, establishment and potential impacts on the economy and biodiversity. The approach has been used in several countries to avail key information about potential biological invasions to risk managers (Sutherland et al. 2008; Gassó et al. 2009; Roy et al. 2014; Bayón and Vilà 2019; Peyton et al. 2019), Spain (Gassó et al. 2009; Bayón and Vilà 2019) and United Kingdom (Sutherland et al. 2008). This information has enabled prevention of introduction through increased awareness to support early-warning and rapid response and contingency planning (Peyton et al. 2020). For some of the pest species provided by the Horizon Scanning Tool, only basic datasheets were available. This affected assessment of risk associated with likelihood of introduction, establishment and potential pathways of introduction. In addition, for most pest species, information on potential socio-economic and environmental impacts is lacking even in enhanced datasheets or completely unavailable. Lastly, information about some of the vectors reported to transmit some of the assessed pathogenic organisms is lacking. For instance, Xylella fastidioda subspecies have been reported to be transmitted by a multitude of vectors, but information on these vectors is not available in SSA. This is why assessment of risk associated with pest species identified through horizon scanning was conducted by SMEs.

The pests that recorded high scores were those reported in Africa and mainly in neighbouring countries or countries with high traffic of trade, such as South Africa, demonstrating that the likelihood of entry is key in determining the overall risk score. More than half of the pests reported as present in Africa were reported in neighbouring countries. This indicates that Zambia needs to ensure that the status of the pests reported as absent in Zambia, but present in neighbouring countries, is correctly established. This will require collaboration of the Plant Quarantine and Phytosanitary Service (PQPS), which is the National Plant Protection Organisation (NPPO), with other key actors, such as public and private research institutions, international research organisations, academia, public and private extension delivery organisations and regional NPPOs.

Soft Rot Pectobacteriaceae (SRP) are one of the most devastating phytopathogenic organisms known to affect a wide range of crops, especially in Solanum tuberosum, Zea mays and a multitude of horticultural crops (Gallois et al. 1992; Adeolu et al. 2016; van der Wolf et al. 2021; Van Gijsegem et al. 2021). The SRPs identified through horizon scanning and assessed included Dickeya chrysanthemi, D. dadantii, D. dianthicola, D. fangzhongdai, D. paradisiaca, D. solani, D. zeae, Pectobacterium aroidearum, P. atrosepticum, P. betavasculorum, P. brasiliense, P. carotovorum, P. cypripedii, P. odoriferum, P. parmentieri and P. polaris, all of which affect S. tuberosum, except, D. zeae, P. cypripedii and P. odoriferum. All these SRPs recorded overall risk scores above 54, except D. fangzhongdai, D. paradisiaca, D. solani, P. aroidearum, P. cypripedii, P. odoriferum and P. polaris majorly because they had not been reported in Africa with the exception of P. cypripedii, which has been reported as present in South Africa. The SRPs that recorded scores above 54 have all been reported in neighbouring countries, except D. dianthicola and P. betavasculorum. It is on this basis that there was a suggestion for detection surveillance to be conducted for these pests before any phytosanitary measure is instituted. However, for the SRPs not recorded in neighbouring countries, detection surveillance was still suggested to confirm pest status, followed by a pest-initiated PRA.

The SRPs that were added because they presented a phytosanitary risk to S. tuberosum value chain included D. oryzae, P. parvum, P. punjabense and P. peruviense. Pectobacterium punjabense is a new species which was recently isolated from S. tuberosum (Sarfraz et al. 2018). This species was added because it is closely related to P. parmentieri, a species that was highlighted through horizon scanning. Pectobacterium parmentieri was reported in the neighbouring country of Zimbabwe and also highlighted as invasive. Both P. parvum and P. punjabense were recently elevated from P. carotovorum, a species highlighted by horizon scanning and reclassified into new species (Waleron et al. 2018; Pasanen et al. 2020). Pectobacterium carotovorum was reported in a number of countries and in the neighbouring country of Zimbabwe. Dickeya oryzae was recently elevated from D. zeae, hence this elevation from a strain that had been highlighted through horizon scanning dictated the inclusion of D. oryzae in the risk assessment process. All the added SRPs recorded low overall risk score because they have not yet been reported in Africa. However, because they have been elevated from SRPs already reported in Africa and more so in neighbouring countries, detection surveillance was suggested to establish pest status.

The xanthomonad, X. citri pv. aurantifolii, was added because, along with Xanthomonas citri pv. citri, both cause Citrus canker disease (CCD) or Asiatic citrus canker (Gottwald et al. 2002; Gabriel et al. 2020; Naqvi et al. 2022). The disease affects several plants in the family Rutaceae particularly Citrus, Fortunella and Poncirus species (da Gama et al. 2018; Naqvi et al. 2022). All known commercial varieties of Citrus have been reported to succumb to the diseases (Gottwald et al. 1989, 2002; Vojnov et al. 2010). The economic impacts due to CCD result from stem die-back, fruit blemishes which affect the quality and eventual price and early fruit drop (Graham 2001; Gottwald et al. 2002). The two pathovars, X. citri pv. aurantifolii and X. citri pv. citri are mainly introduced into new geographical areas through the transportation of infected fruits from infested zones to production areas free of the disease (Gottwald et al. 2002; Naqvi et al. 2022). The two pathovars are considered quarantine organisms in most countries where they have not yet been reported (Schubert et al. 2001; Gottwald et al. 2002; Naqvi et al. 2022), hence the overall risk score of 75 and 100 for X. citri pv. aurantifolii and X. citri pv. citri, respectively, was enough to instigate a suggestion of surveillance since X. citri pv. citri had been recorded in the neighbouring country of Tanzania.

One of the emerging bacterial pathogenic species of economic importance, Xylella fastidiosa that has now been reported in America, Asia, Europe and Oceania, but not yet in Africa, was also assessed (Baldi and La Porta 2017; Rapicavoli et al. 2018). Xylella fastidiosa is divided into three main subspecies, each with a specific host range, X. fastidiosa subsp. fastidiosa which causes Pierce’s disease; X. fastidiosa subsp. multiplex which causes almond leaf scorch and phony peach disease; and X. fastidiosa subsp. pauca which causes citrus variegated chlorosis and olive quick decline syndrome (Sanderlin 2017; Rapicavoli et al. 2018; Greco et al. 2021). Three other subspecies, although of limited economic importance and host spectrum, also cause X. fastidiosa disease symptoms. They are X. fastidiosa subsp. morus, X. fastidiosa subsp. sandyi which causes oleander leaf scorch and X. fastidiosa subsp. tashke which causes leaf scorch in Chitalpa tashkentensis (Schuenzel et al. 2005; Randall et al. 2009; Nunney et al. 2014; Rapicavoli et al. 2018). The three major subspecies and X. fastidiosa subsp. sandyi were picked through horizon scanning and assessed. Two of these subspecies, X. fastidiosa subsp fastidiosa and X. fastidiosa subsp. pauca affect crop species (Citrus sinensis and Coffee. arabica) (Marucci et al. 2008; Bergsma-Vlami et al. 2017; Esteves et al. 2020) that are key to the Zambian economy. Xylella fastidiosa has the capacity to rattle the trading capacity of any country. It is a quarantine pest in most of Europe, the destination of agricultural produce from Africa and, therefore, it is essential that it is kept out of Zambia and other African countries.

Based on the results from the rapid risk assessment, the following recommendations are suggested; (1) conduct detection surveillance especially for pests reported in neighbouring countries to establish pest status before any further action, such as developing pest-initiated PRAs is conducted. Where the pest is established as present, a delimiting survey is suggested to establish the boundaries of infestation. Although not yet detected in Africa, periodic surveillance for X. fastidiosa should be conducted. It is also essential for funds to be allocated to conduct research on the likely vectors of this pathogen; (2) Pest-initiated PRA should be conducted for pests that cause high economic damage or may endanger trade in value chains key to the Zambian economy; (3) The risk associated with the assessed pests needs to be reviewed periodically to establish any changes and devise necessary mitigation measures. The suggested periodic review will require the establishment of a pest risk register to which these bacteria and protist species will be added. The risk registers are developed, based on the concept by the United Kingdom’s Plant Health Risk Register ⁹, Northern Ireland’s Plant Health Risk Register ¹⁰ or Finland’s FinnPRIO-Explorer ¹¹. Lastly, the results from this assessment will support the updating of the list of regulated pests. The actions suggested will be implemented by the Zambian NPPO, Plant Quarantine and Phytosanitary Service (PQPS) working with key actors in Extension, Research and Academia.

This work was financially supported by the Foreign, Commonwealth and Development Office (FCDO), United Kingdom, the Directorate-General for International Cooperation (DGIS), Netherlands, the European Commission Directorate-General for International Cooperation and Development (DEVCO) and the Swiss Agency for Development and Cooperation (SDC) through CABI’s PlantwisePlus Programmes. CABI is an inter-governmental, not-for-profit organisation and we gratefully acknowledge the core financial support from our member countries and lead agencies.