Phytosanitary risk associated with illegal importation of pest-infested commodities to the South African agricultural sector

AFFILIATIONS: 1Directorate: Plant Health, Department of Agriculture, Land Reform and Rural Development, Pretoria, South Africa 2Directorate: Biosecurity, Department of Forestry, Fisheries and the Environment, Cape Town, South Africa 3Department of Biodiversity, University of Limpopo, Polokwane, South Africa 4School of Agricultural, Earth and Environmental Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa


Introduction
Introduction of alien and invasive species into regions outside of their native ranges can have undesirable effects on both ecosystem and agriculture. 1 Most countries, including South Africa, are currently facing threats from the introduction, spread and establishment of alien and invasive species. Various countries are struggling to prevent the influx of further alien and invasive species as the global economy expands and the movement of goods, services and people continues to grow. 2 A primary means by which alien and invasive species become established is through unintentional introductions associated with international trade. 3 These invasive alien species can have an exceedingly broad range of economic, environmental and social impacts. 4,5 International trade of plants and plant products is one of the major pathways for the introduction and spread of exotic pests. Some of these pests may affect agricultural production and/or limit access to international export markets. Phytosanitary inspections of plants and plant products at border ports are an important phytosanitary practice to determine the levels of compliance with phytosanitary requirements. To reduce phytosanitary risk, trading partners adhere to rigorous measures for import or export to avoid the introduction of alien and invasive species to new regions. Alien and invasive species are common stowaways on shipments of imported plants, plant products and other regulated articles. 6,7 Alien and invasive species may arrive on imports encompassing a variety of commodities, including agricultural produce, greenhouse and ornamental plants, nursery stock, cut flowers, wood products, stored products and packing materials. 8,9 Global air transportation and road transportation greatly facilitate the unintended spread of pests, including invasive species, because of the large volumes of goods and people transported internationally 10 which also are gradually increasing every year 11 . Given the tremendous increases in global passenger travel, there is a need to better characterise the extent to which passenger baggage serves as an invasion pathway for alien and invasive species. 12 In South Africa, the potential introduction of pests and diseases is administered through the Agricultural Pests Act No. 36 of 1983 and its associated regulations 13 , National Environmental Management: Biodiversity Act No. 10 of 2004 14 , and Alien and Invasive Species Regulation (2014) as amended 14 . The Acts deal with prevention and control of the introduction and spread of pests. The Agricultural Pests Act compels imported controlled goods to be declared and presented at ports of entry to the executive officer and/or authorised inspector who then inspects or samples the controlled goods as necessary. The inspection and sampling are done to determine the presence of regulated pests in a commodity. Regulated pests include both quarantine and non-quarantine pests. 15 The Directorate: Inspection Services and Directorate: Plant Health within the South African Department of Agriculture, Land Reform and Rural Development (DALRRD) are responsible for inspections, policy development and implementation. The inspectors from DALRRD ensure that imported controlled goods are free from non-indigenous organisms, including phytophagous insects, mites, molluscs, nematodes, plant pathogens and invasive weed species. The Directorate: Inspection Services conducts inspections of baggage carried by international travellers or passengers that arrives at South African ports and borders, primarily focusing on plant commodities which could likely harbour live plant pests. These inspections were conducted for 8 years (2011-2019). The Directorate: Plant Health publishes and maintains the database of intercepted pests.
The purpose of this study was to determine the trend associated with the interception of pests in passengers' baggage at South African borders and airports. We examined the origins of imported commodities, pests intercepted, status of intercepted organisms in South Africa and the likelihood of establishing in South Africa, as a critical effort to prevent negative impacts on the economy, ecosystems and agriculture through the possible introduction and spread of quarantine species.

Sample collection and preparation
Plant commodities intended for import into South Africa and illegally moved were confiscated by the DALRRD. Samples (n=341) from various specimens were collected over a period of 8 years (2011-2019) from O.R. Tambo International Airport (Johannesburg) and nine border posts (Vioolsdrift, Nakop, Grobler's Bridge, Skilpad's Gate, Ramatlabama, Beit Bridge, Lebombo, Oshoek and Golela). The samples were then sent to the DALRRD Diagnostic Laboratories in Pretoria (Gauteng Province) and Stellenbosch (Western Cape Province) for pest identification. In cases in which identification could not be made with certainty, the specimens were sent to the Biosystematics Division of the Agricultural Research Council (Pretoria) for further identification to species level. Immature and damaged specimens were identified to only genus or family level.

Data analysis
Data and information regarding commodity species name, commodity type, pests detected, pests' quarantine status and country of origin were analysed descriptively using Statistical Software Package Version 2010 (Statsoft Inc., Tulsa, OK, USA).
Based on the risk, intercepted pests were divided into quarantine, potential quarantine, non-quarantine and uncategorised (N/A) pests. In terms of pest status in South Africa, most of the intercepted organisms were non-quarantine species (70.50%), pests of unknown status (17.28%), quarantine pests (10.84%) and potential quarantine pests (1.35%) ( Figure 1). Prostephanus truncatus Horn (larger grain borer), P. citricarpa, B. dorsalis and S. frugiperda were the only quarantine pests intercepted from imported grains and fresh fruits ( Table 2), but these pests have a high disaster risk to the South African agricultural sector as well as the economy. Pests of unknown status have a high potential to negatively affect agricultural production.
The highest frequency of pest interceptions occurred on commodities imported mainly from Mozambique (47%), followed by Zimbabwe (15%) and Eswatini (12%). The frequency of interceptions from Spain, France, Ukraine, Malawi, Ethiopia, Nigeria, Ghana, Mauritius, Zambia, USA and Israel was between 1% and 5%, while countries such as New Zealand, Angola, Kenya, DRC, Jordan, India, Russia and Namibia accounted for less than 1% (Table 3).

Discussion
The majority of pests intercepted were non-quarantine pests ( Figure 1); however, these pests may also pose a risk in the agricultural sector by threatening food security and production. In terms of international and national prescripts, only regulated pests and/or quarantine pests are subject to phytosanitary measures. 16 This is because the introduction and spread of quarantine pests may destroy the agricultural and horticultural sectors. The introduction and spread of quarantine pests and pests of unknown status may ultimately affect the environment, economy, food security as well as export markets. 17 It could lead to agricultural production losses of 20-40% 18 and further increase the cost of operations and disease control.
In most cases, the entry and introduction of plant pests of economic importance from other countries into South Africa is through the movement of plants and plant products during international trade and/or movement of people with commodities. Most alien and invasive species are introduced and/or intercepted during international trade worldwide. 19 It is thus important that plant pest interception is appropriately dealt with in accordance with phytosanitary measures and actions. In South Africa, according to the Agricultural Pests Act, ports of entry are prescribed under Regulations R.111 of 27 January 1984 and Government Notice R.1013 of 26 May 1989 as amended, wherein plant commodities are permitted to be imported. 13 This legislation requires all importers of plant products to comply with South Africa's import requirements and plant products are subject to inspection at the prescribed ports of entry.
In other countries, such as those in the European Union, alert lists on fruits have been established to manage the risk. 20 In South Africa, the majority of intercepted pests is found to be non-quarantine pests (Figure 1), and thus they are not subjected to phytosanitary measures. However, the majority of pests that have entered and been introduced into South Africa are pests of economic importance. This implies that the import procedures as well as the regulatory systems of South Africa need to be improved and strengthened. 21 Although there are regulatory frameworks to regulate the importation of plant products in the Republic of South Africa, passengers still disregard the rules and manage to bypass the system with unauthorised commodities or by importing commodities that do not comply with South African import requirements. This study revealed that these activities normally happen at land borders (as opposed to the airport) where South Africa shares the borders with neighbouring countries such as Eswatini, Zimbabwe and Mozambique. The DALRRD should take decisive action in terms of plant health awareness as well as in enforcing the law at the ports of entry to ensure that a high level of compliance is realised. The Agricultural Pests Act requires that illegally imported plant products should be subject to confiscation and destruction, and offenders should be subject to Section 13 of the Act, which deals with 'offences and penalties'.     Currently, the DALRRD is undergoing a review of the Agricultural Pests Act in relation to phytosanitary measures so that there is better alignment with internationally prescribed export and import provisions. The approval of the proposed bill (Plant Health (Phytosanitary) Bill) could limit the introduction of exotic pests. The provisions of the proposed bill also provide for on-the-spot fines for non-compliance. 22 This approach is not new; the Australian government has imposed on-the-spot fines and/ or penalties for non-compliance since 2009 under the Plant Health Act, 2009 and this mechanism is working effectively to reduce smuggling and/or illegal imports of plant commodities. 23 South African borders still lack relevant equipment such as scanners to detect undeclared plant products during movement of people crossing South African borders. Therefore, the majority of passengers with unauthorised plant products and/or fruits pass through undetected, as indicated by the high number of interceptions in this study. Currently, South Africa employs sniffer dogs in other ports of entry to detect plant commodities in passengers' luggage. However, these remain limited and need to be increased across all ports of entry in order to reduce the introduction of pests through undeclared and/or non-compliant plant commodities. The system may be further intensified at ports of entry with the establishment of the new South African Border Management Authority under the Border Management Act, 2020 (Act No. 2 of 2020).
Based on our results, adequate measures are required at South Africa's land borders, particularly for imported fruits. The majority of illegal imports and pest interceptions occurred from Mozambique, Zimbabwe and Eswatini (Table 3), which thus require the most stringent measures to be put in place to prevent the introduction of pests. The challenge is not only in South Africa -all African borders are under enormous pressure due to the movement of people and goods across borders. 24 In contrast, in the USA, the highest number of pest interceptions was recorded at the airports, followed by the land border between the USA and Mexico. 25 The results from this study suggest that imported fruits followed by grains are the commodities with the highest levels of interception of quarantine pests into South Africa from neighbouring countries. Fruits are also the major pathway of pests and disease worldwide. 26 The majority of countries, including South Africa, import fruits in large volumes. Insects and/or pests hide, grow and reproduce in those imported fruits, which are latter intercepted by the receiving country. 6 This implies that fresh produce (fruits and vegetables) is the major pathway for actionable pests in the USA 27 as well as in South Africa.
We have demonstrated a high phytosanitary risk associated with the illegal importation of plant commodities. Amongst the intercepted organisms, the quarantine pests were B. dorsalis, S. frugiperda, P. citricarpa and P. truncatus, which occur in South Africa but are currently under official control in terms of the Agricultural Pests Act. According to the International Plant Protection Convention, a quarantine pest is 'a pest of potential economic importance to the area endangered thereby and not yet present there, or present but not widely distributed and being officially controlled'.
The discovery of B. dorsalis on the African continent during 2003 raised biosecurity concerns in South Africa where agriculture is of major socio-economic importance. 28 This is a pest species that has recently been introduced into eastern Africa and has subsequently made a rapid expansion across tropical Africa. 29 B. dorsalis is highly polyphagous 30,31 , it has more than 40 known cultivated and wild hosts in Benin 32 , and is expected to have a broad host range as exhibited by some other members in the B. dorsalis complex. Female individuals can lay an average of 1300 eggs during their lifetimes, depending on the host and climatic conditions. The species is multivoltine with an average life span of about 3 months. 33 Given the apparently rapid spread of B. dorsalis across Africa, and its impacts on local horticulture, the possibility of this species being introduced to, and establishing in and invading other regions of the world, should be prevented. 34 38 In Ethiopia, maize infestation of this insect pest was estimated to range from 24% to 39%, while in Kenya, the infestation was about 3854%. 39 Fall armyworm caused reductions in maize yields of 934 kg/ha and 1381 kg/ ha in Ethiopia and Kenya, respectively. 39 Farmers in Ethiopia and Kenya observed a more than 82% increase in the spread of fall armyworm on their farms. The Ethiopian and Kenyan farmers reported fall armyworm as a serious insect pest, which caused a higher level of damage than the maize stalk borer. 39 Another intercepted pest found in the current study was the citrus black spot pathogen, P. citricarpa, which is a fungal pathogen of citrus plants, specifically orange and lemon varieties. 40 In South Africa, citrus fruit exports to European and US markets are subjected to strict phytosanitary measures. 41 Internationally, P. citricarpa is considered a quarantine pathogen. 42 Citrus black spot occurs in citrus-growing regions with warm summer rainfall climates. 43 The larger grain borer, P. truncatus, was also detected in the current study and is regarded as an economically important pest of stored commodities such as maize and dried cassava. 44 This pest is endemic to Mexico and Central America, although it has recently been introduced and become established on the African continent, where it has caused severe damage to stored maize. The first outbreaks were reported in the Eastern part of Africa. 45 P. truncatus became established in Togo in 1984, and gradually spread to Benin, Burkina Faso, Niger, Nigeria, Guinea Conakry and Guinea Bissau. 46 The economic impact of insect pest attacks on stored grain is associated with the amount of grain damaged or the percentage weight loss. 47 In Zimbabwe, it was first reported in Mashonaland West and Mashonaland Central Provinces, with potential distribution from the northern part of the country moving further inland towards the central and eastern parts, and neighbouring countries such as South Africa, Zambia and Mozambique. 48,49

Conclusion
The risks posed by the illegal introduction of pests through a particular plant commodity should also be considered in a pest risk analysis, because even though the commodity itself may not pose a pest risk, it may harbour organisms that have pests. Therefore, illegal importation of plant and plant products into South Africa should undergo a high phytosanitary risk assessment. The introductions of alien and invasive pests into South Africa can have undesirable effects on the ecosystem, agriculture, biodiversity as well as the economy. The highest number of pest interceptions occurred on fresh fruits, grains and vegetables mainly from southern African countries, particularly Mozambique, Zimbabwe and Eswatini. Although the majority of intercepted pests were nonquarantine species, the consequences due to repeated interceptions of quarantine pests should be taken into consideration. The agricultural sector, particularly citrus, maize, fruit and vegetable industries in South Africa, could be under severe threat from the establishment and spread of quarantine pests such as P. citricarpa, B. dorsalis, S. frugiperda and P. truncatus to areas where these do not occur. In addition, consignments presented for import into South Africa must be subject to pre-import phytosanitary inspection. As an economic consequence, fresh produce farmers in areas free from these pests stand to spend more money in eradicating these pests if they are introduced and/or established. Many people stand to lose jobs as farmers will be reducing their workforce because of reduced profits. Crop production, biodiversity, food security, existing export markets, and access to new export markets could also be threatened as importing countries may impose stringent phytosanitary measures to limit the chances of introduction and establishment of these quarantine pests into their territories.
South Africa is a signatory member of the World Trade Organisation Agreement on the Application of Sanitary and Phytosanitary Measures and the International Plant Protection Convention. These international organisations acknowledge the sovereign right of Members to protect the life and health of plants within their territories by means of phytosanitary regulatory controls. The spread of quarantine pests to new areas where they have not previously occurred can lead to severe crop production losses and food insecurity.