Invasive alien species (IAS) continue to shape the global landscape through their effects on biological diversity and agricultural productivity. The effects are particularly pronounced in Sub-Saharan Africa, which has seen the arrival of many IAS in recent years. This has been attributed to porous borders, weak cross border biosecurity, and inadequate capacity to limit or stop invasions. Prediction and early detection of IAS, as well as mechanisms of containment and eradication, are needed in the fight against this global threat. Horizon scanning is an approach that enables gathering of information on risk and impact that can support IAS management. A study was conducted in Ghana to establish two ranked lists of potential invasive alien plant pest species that could be harmful to agriculture, forestry, and the environment, and to rank them according to their potential threat. The ultimate objective was to enable prioritization of actions including pest risk analysis, prevention, surveillance and contingency plans. Prioritisation was carried out using an adapted version of horizon scanning and consensus methods developed for ranking IAS worldwide. Following a horizon scan of invasive alien species not yet officially present in Ghana, a total of 110 arthropod and 64 pathogenic species were assessed through a simplified pest risk assessment. Sixteen species, of which 14 were arthropods and two pathogens, had not been recorded on the African continent at the time of assessment. The species recorded in Africa included 19 arthropod and 46 pathogenic species which were already recorded in the neighbouring countries of Burkina Faso, Côte d’Ivoire, and Togo. The majority of arthropod species were likely to arrive as contaminants on commodities, followed by a sizable number which were likely to arrive as stowaways, while some species were capable of long distance dispersal unaided. The main actions suggested for species that scored highly included full pest risk analyses and, for species recorded in neighbouring countries, surveys to determine their presence in Ghana were recommended.

Horizon scanning, invasive arthropods, pathogens, pathway of introduction, pest prioritisation, pest risk analysis

The spread of invasive alien species (IAS) has been increasing exponentially over the years, greatly facilitated by international trade and the global transport industry (Perrings et al. 2005; Meyerson and Mooney 2007). The International Union for the Conservation of Nature (IUCN) defines an alien species as a species, subspecies, or lower taxon introduced outside of its natural range and dispersal potential, i.e. outside the range it occupies naturally or could not occupy without intentional or unintentional introduction or care by humans (IUCN 2000). An alien species becomes invasive once it threatens biological diversity, food and economic security, and human health and well-being (Meyerson and Mooney 2007). In particular, IAS can cause significant economic damage through their negative effect on crop harvests and the sustainability of rural economies, thereby threatening livelihoods of hundreds of millions of people, especially in the developing world (Paini et al. 2016; Pratt et al. 2017).

In recent years, Sub-Saharan Africa (SSA), a region dominated by resource-poor farmers, has suffered from an increasing number of invasive plant pests. Eschen et al. (2021) estimated that the annual cost of IAS to agriculture in Africa reaches USD 65.58 Bn per year, with yield losses, reductions in livestock derived income and IAS management costs, mainly labour costs, constituting most of the estimated losses. In their study, the pest causing the highest yield losses (USD 9.4 Bn) was the fall army worm (Spodoptera frugiperda). This American pest was first recorded in Africa in 2016 and has since spread to SSA, threatening smallholder maize and sorghum production (De Groote et al. 2020; Tambo et al. 2020). Plant pathogens are also extremely damaging. For example, maize lethal necrosis, a disease caused by co-infection of Maize chlorotic mottle virus and Sugarcane mosaic virus was first reported in Kenya in 2011 but has since been reported in Democratic Republic of Congo, Ethiopia, Rwanda, and Tanzania (Mahuku et al. 2015; Mengesha et al. 2019; Kiruwa et al. 2020). The disease has had devastating effects on maize production in SSA (Mahuku et al. 2015; Boddupalli et al. 2020). Other plant pests recently reported in the region with devastating effects include tomato pinworm (Tuta absoluta) (Mansour et al. 2018), Cassava brown streak virus (Ferris et al. 2020), wheat stem rust (Puccinia graminis f. sp. tritici) (Fetch et al. 2016) and potato cyst nematodes (Globodera rostochiensis and G. pallida) (Mwangi et al. 2015; Mburu et al. 2020).

Increased trade between countries and regional blocks on the African continent has resulted in the spread of IAS once they have been reported on the continent (Nagoshi et al. 2018). It should also be noted that not all IAS invade Africa from overseas; some may be native to parts of Africa but are intentionally or unintentionally introduced to some countries or spread across the continent (Gezahgne et al. 2005; Roux and Coetzee 2005; Nakabonge et al. 2006). The spread of IAS from overseas and within the continent can be attributed to porous borders, weak cross border biosecurity, and inadequate capacity to limit or stop invasions (Early et al. 2016; Kansiime et al. 2017; Nagoshi et al. 2018; Graziosi et al. 2020). This exposes Africa both to repeated invasions from novel diseases, invertebrate pests and weeds and to continued spread across the continent once they have arrived (Day et al. 2017). Successful management of IAS involves prevention or early detection of invasions and ensuring effective management in case of arrival (Hulme 2006). Prevention of invasions remains the most cost-effective option of reducing impact of IAS (Wittenberg and Cock 2001; Leung et al. 2002). However, this requires an assessment of the highest risk species to enable the management of pathways of introduction, interception of movements at border points, and assessment of risk for planned imports (Simberloff et al. 2013). Once prevention fails and an IAS enters any jurisdiction, early detection, which allows for cost-effective removal, is important to institute eradication and containment interventions (Wittenberg and Cock 2001; Keller et al. 2007).

Horizon scanning for invasive species is an approach that provides countries with opportunities to gather information about IAS likely to head in their direction (Peyton et al. 2019). It involves the systematic search for potential IAS, their impacts on biodiversity, the potential to harm biodiversity, economic activities and human health, and opportunities for impact mitigation (Roy et al. 2014, 2019; Peyton et al. 2019, 2020). It is an important tool that contributes to prevent arrival, early identification and eradication of an IAS and is an essential component of IAS management with demonstrated net economic and ecological benefits (Keller et al. 2007; Caffrey et al. 2014). Horizon scanning has been used to determine the potential arrival, establishment and impact of invasive alien species in Europe (Roy et al. 2014, 2019; Gallardo et al. 2016; Peyton et al. 2019) and provides a practical and affordable option for African countries. The objective of this study was to employ horizon scanning to, firstly, establish a list of potential invasive alien plant pests (arthropods including insects and mites, and pathogens including fungi, bacteria, fungi and nematodes) that are considered not yet present in Ghana but may be harmful to Ghana’s agriculture, forestry or environment if introduced. Secondly, to rank these arthropods and pathogens according to their potential threat, which will allow to prioritise actions including pest risk analysis, prevention, surveillance and contingency plans to mitigate the negative effects of introduced species (Peyton et al. 2019; Roy et al. 2019).

The prioritisation was carried out by a panel of 23 Subject Matter Experts (SMEs) from Ghana research institutions and academia with experience in entomology, bacteriology, mycology, nematology and virology. An adapted version of the consensus method developed for ranking IAS (Sutherland et al. 2011; Roy et al. 2014) was used to derive a ranked list of invertebrates and pathogens harmful to plants and likely to enter Ghana in the near future. The approach involved the following steps:

The full results of the assessments are provided in the Suppl. material 2 while the 40 species with the highest scores are provided in Table 1 and Table 2, which also presents the most suitable actions to be taken against them.

The prioritization method used in this study was inspired from horizon scanning and prioritization of IAS (Roy et al. 2014, 2017, 2019; Bayón and Vilà 2019) and was used successfully to create two separate ranked lists of alien plant pests according to their potential threat for Ghana and to prioritize actions. The species with the highest scores were mostly those that scored high in the likelihood of entry, i.e. mostly those that were already recorded in neighbouring countries or spreading rapidly in Africa. It is logical that these species are prioritised and immediate actions taken through organising surveillance programmes. Species that were far from the country and were not spreading rapidly had a lower entry score that impacted the overall score, even though they could have serious effects if they arrived in Ghana. Examples of these species scoring low in likelihood of entry but high in impact included two cocoa pathogens, Moniliophthora roreri, the cause of frosty pod rot of cocoa (Phillips-Mora and Wilkinson 2007; Bailey et al. 2018) and M. perniciosa which causes “Witches broom disease” in cocoa (Meinhardt et al. 2008; Lisboa et al. 2020). Although M. roreri causes lower losses than some pathogens on a global scale due to its limited range, its economic impact in any epidemic ranks among the major pod pathogens (Ploetz, 2016). It is also ranked among the main yield‐limiting factors of cocoa production in tropical America (Bailey et al. 2018). Severe outbreaks of M. roreri have resulted in abandonment of cocoa cultivation in extensive areas of Peru, Costa Rica, Colombia and Mexico (Phillips-Mora and Wilkinson 2007). In the 1970s, Moniliophthora perniciosa caused pod losses exceeding 90% in Rondonia, a Brazilian State, causing a significant socio-economic impact on the development of that State (Lisboa et al. 2020). In the State of Bahia, the pathogen was deliberately introduced in what is now considered an act of terrorism (“agro-terrorism”), which caused a reduction in production by almost 70% within 10 years (Saatchi et al. 2001; Caldas and Perz 2013; Lisboa et al. 2020).

The likelihood of establishment played a less important role in the prioritisation because species that are unlikely to establish because of unsuitable climate or absence of host plants were excluded in the preliminary sorting. Thus, most species scored high in the likelihood of establishment. The impact score also played an important role in the overall score, but mostly through their potential economic impact. Few species scored high in environmental impact, probably because most invasive plant pests in tropical regions are rather known for their economic impact and those that cause concern for non-commercial plants attract less attention and may pass under the radar of such horizon scanning. Many invasive arthropods are also known for their environmental impact (Kenis et al. 2009), but most of these are invasive predators such as ants and ladybirds, or pollinators. Nevertheless, some alien herbivorous arthropods and plant pathogens also have huge impacts on biodiversity and ecosystem functions worldwide, in particular those affecting tree species such as emerald ash borer, which has killed tens of millions of ash (Fraxinus spp.) in North America (Herms and McCullough 2014), hemlock woolly adelgid causing the decline of hemlock (Tsuga spp.) in North America (Ellison et al. 2018), box tree moth, which decimates wild box stands (Buxus sempervirens) in Europe (Mitchell et al. 2018), and the pathogens causing chestnut blight (Rigling and Prospero 2018), Dutch elm disease (Harwood et al. 2011), and ash dieback (Mitchell et al. 2014), which have had a dramatic impact on chestnut (Castanea spp.), elm (Ulmus spp.) and ash, respectively, in North America and Europe. Some serious invasive tree pests such as the sirex woodwasp (Sirex noctilio) (Tribe and Cillié 2004), Eucalyptus long-horned borers (Phoracantha semipunctata and P. recurva) (Paini et al. 2016), Cypress aphid (Cinara cupressi) (Watson et al. 1999), Coniothyrium stem canker (Gezahgne et al., 2005) and pink disease caused by Erythricium salmonicolor (Roux and Coetzee 2005) have also been recorded in Africa but mostly concern exotic trees. An exception is Euwallacea fornicatus, a wood-boring beetle from Asia that damages many native trees in South Africa (Paap et al. 2018).

Several alien arthropods and pathogens were identified in neighbouring countries, which suggests that some of these species may already be present in Ghana but have not yet been recorded or identified to the species level. It is essential that these species are sampled and identified using morphological and molecular methods. This could be the case for some species that reached high scores in the assessment. For instance, Maconellicoccus hirsutus is a scale insect that is a serious pest of cocoa (Fornazier et al. 2017), a key crop in Ghana. It is present in all three neighbouring countries, but not yet officially reported in Ghana. Another typical example is that of the leaf mining flies of the genus Liriomyza (Parrella 1987; Lee et al. 2004; Migiro et al. 2010). Three species of this genus, L. trifolii, L. huidobrensis and L. sativae, are notorious for being invasive and all are alien in Africa (Radcliffe and Lagnaoui 2007; Migiro et al. 2010; Akutse et al. 2013; EFSA Panel on Plant Health et al. 2020b). However, so far, only “Liriomyza sp.” has been reported in Ghana (Garmonyou et al. 2014) although L. sativae has been intercepted in the European Union on products from Ghana, suggesting that it is present in the country (EFSA Panel on Plant Health et al. 2020b). Similarly, the highly invasive thrips, Thrips palmi (Cannon et al. 2007; EFSA Panel on Plant Health et al. 2019) is reported from neighbouring countries and it is known that Thrips spp. cause serious damage to vegetables in Ghana (Baah et al. 2015), but it is not clear what species are present in the country. The whitefly Bemisia tabaci is known to be a complex of many sibling species, several of them being highly invasive worldwide (Perring 2001; Vyskočilová et al. 2018). These species can only be identified using molecular tools (Vyskočilová et al., 2018) and it is not clear to which species of the Bemisia tabaci complex the numerous records in Ghana refer.

Species that are most probably not yet present in Ghana but already in neighbouring countries or spreading fast on the continent may require implementation of surveillance programmes, which could either be based on visual surveys or trapping campaigns (Berec et al. 2015; Ward et al. 2016). An example is Spodoptera eridania, found in Africa in 2016 and already present in several African countries including Nigeria and Benin (Goergen 2018; EFSA Panel on Plant Health et al. 2020a). There is uncertainty regarding the risk of several species, either because the likelihood of entry and establishment is unclear or because the potential impact is difficult to assess. In such cases, a full PRA would be needed. Pest risk analyses may also be needed for species that are undoubtedly considered as high-risk pests but require quarantine measures that can only be justified based on full PRAs carried out following international standards.

When assessing risks, it is important to supplement the answers with a confidence level, or a level of uncertainty (Holt et al. 2014). Our simplified PRA system asked assessors to provide a confidence level for the answers, both for the single scores and for the overall score. However, the overall confidence level provided by the entomology and pathology groups (Suppl. material 2) were very different, i.e. the pathology group considering that the overall scores for pathogens and nematodes were obtained mostly with high confidence whereas the entomology group was more cautious and provided mostly medium confidence levels for arthropods, although there is no reason to believe that data on arthropods are less reliable than those on pathogens and nematodes. Moreover, the levels of confidence provided by the different assessors for the same questions using the same information sources often differed from high to low, suggesting that, in the future, instructions for the scoring of confidence levels should be more clearly defined.

We have demonstrated that through horizon scanning, a country can identify potential invasive plant pests, both invertebrates and pathogens, and use the information to determine the risk associated with each. This will enable the country to invest the limited resources in priority actions such as preventing arrival and establishment of IAS, PRAs, surveillance and developing contingency plans. This study can serve as a model for future projects on plant pests’ prioritisation in Africa and elsewhere. It would be applicable for assessing the risk of invasive plant pests in any country or region, e.g. trade blocks, with minor modifications of the method, particularly in the mini-PRA protocol used to score species.

This study was financially supported by the Foreign, Commonwealth and Development Office (FCDO), UK, 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 Action on Invasives and Plantwise Plus Programmes. CABI is an international intergovernmental organisation and we gratefully acknowledge the core financial support from our member countries and lead agencies. See https://www.cabi.org/aboutcabi/who-we-work-with/key-donors/ for details.