Pest categorisation of Spodoptera frugiperda

1.1.1 Background

Council Directive 2000/29/EC on protective measures against the introduction into the Community of organisms harmful to plants or plant products and against their spread within the Community establishes the present European Union plant health regime. The Directive lays down the phytosanitary provisions and the control checks to be carried out at the place of origin on plants and plant products destined for the Union or to be moved within the Union. In the Directive's 2000/29/EC annexes, the list of harmful organisms (pests) whose introduction into or spread within the Union is prohibited, is detailed together with specific requirements for import or internal movement.

Following the evaluation of the plant health regime, the new basic plant health law, Regulation (EU) 2016/2031 on protective measures against pests of plants, was adopted on 26 October 2016 and will apply from 14 December 2019 onwards, repealing Directive 2000/29/EC. In line with the principles of the above mentioned legislation and the follow-up work of the secondary legislation for the listing of EU regulated pests, EFSA is requested to provide pest categorizations of the harmful organisms included in the annexes of Directive 2000/29/EC, in the cases where recent pest risk assessment/pest categorisation is not available.

1.1.2 Terms of Reference

EFSA is requested, pursuant to Article 22(5.b) and Article 29(1) of Regulation (EC) No 178/2002, to provide scientific opinion in the field of plant health.

EFSA is requested to prepare and deliver a pest categorisation (step 1 analysis) for each of the regulated pests included in the appendices of the annex to this mandate. The methodology and template of pest categorisation have already been developed in past mandates for the organisms listed in Annex II Part A Section II of Directive 2000/29/EC. The same methodology and outcome is expected for this work as well.

The list of the harmful organisms included in the annex to this mandate comprises 133 harmful organisms or groups. A pest categorisation is expected for these 133 pests or groups and the delivery of the work would be stepwise at regular intervals through the year as detailed below. First priority covers the harmful organisms included in Appendix 1, comprising pests from Annex II Part A Section I and Annex II Part B of Directive 2000/29/EC. The delivery of all pest categorisations for the pests included in Appendix 1 is June 2018. The second priority is the pests included in Appendix 2, comprising the group of Cicadellidae (non-EU) known to be vector of Pierce's disease (caused by Xylella fastidiosa), the group of Tephritidae (non-EU), the group of potato viruses and virus-like organisms, the group of viruses and virus-like organisms of Cydonia Mill., Fragaria L., Malus Mill., Prunus L., Pyrus L., Ribes L., Rubus L. and Vitis L.. and the group of Margarodes (non-EU species). The delivery of all pest categorisations for the pests included in Appendix 2 is end 2019. The pests included in Appendix 3 cover pests of Annex I part A section I and all pests categorisations should be delivered by the end of 2020.

For the above mentioned groups, each covering a large number of pests, the pest categorisation will be performed for the group and not the individual harmful organisms listed under “such as” notation in the Annexes of the Directive 2000/29/EC. The criteria to be taken particularly under consideration for these cases, is the analysis of host pest combination, investigation of pathways, the damages occurring and the relevant impact.

Finally, as indicated in the text above, all references to ‘non-European’ should be avoided and replaced by ‘non-EU’ and refer to all territories with exception of the Union territories as defined in Article 1 point 3 of Regulation (EU) 2016/2031.

2.1.1 Literature search

A literature search on S. frugiperda was conducted at the beginning of the categorisation in the ISI Web of Science bibliographic database, using the scientific name of the pest as a search term. Relevant papers focusing on geographic distribution, general biology and life cycle, host plants and the damage it causes were reviewed. Further references and information were obtained from citations within the references and grey literature.

2.1.2 Database search

Pest information, on host(s) and distribution, was retrieved from the EPPO Global Database (EPPO, 2017a,b) and the CABI Crop Protection Compendium (CABI, 2017) and further updated with reports compiled in Abrahams et al. (2017).

Data about import of commodity types that could potentially provide a pathway for the pest to enter the EU and about the area of hosts grown in the EU were obtained from EUROSTAT.

The Europhyt database was consulted for pest-specific notifications on interceptions and outbreaks. Europhyt is a web-based network launched by the Directorate General for Health and Consumers (DG SANCO), and is a subproject of PHYSAN (Phyto-Sanitary Controls) specifically concerned with plant health information. The Europhyt database manages notifications of interceptions of plants or plant products that do not comply with EU legislation, as well as notifications of plant pests detected in the territory of the MSs and the phytosanitary measures taken to eradicate or avoid their spread.

3.1.1 Identity and taxonomy

S. frugiperda (J.E. Smith, 1797) is an insect in the order Lepidoptera and the family Noctuidae. It is known in English as fall armyworm, corn leafworm, and southern grassworm; in French as légionnaire d'automne; in German as Heerwurm, and in Spanish as cogollero del maíz.

There was a revision of the world Spodoptera by Pogue (2011) but the taxonomy of species within the genus is still an area of ongoing research, e.g. Juárez et al. (2014), Dumas et al. (2015a,b), Hanniger et al. (2017). Two morphologically identical strains of S. frugiperda are recognised, commonly referred to as the corn strain and the rice strain, due to host preferences. There is a high level of genetic differentiation between the strains (Pashley, 1986; Kergoat et al., 2012; Juárez et al., 2014) as well as differences in diurnal mating pattern (Schöfl et al., 2009; Hanniger et al., 2017) and differences in female sex pheromones (Lima and McNeil, 2009). Drès & Mallet (2002) considered the rice- and corn-associated S. frugiperda as separate species. Prowell et al. (2004) suggested that they were recently evolved species that are not completely reproductively isolated. Other authors suggest that S. frugiperda is still in the process of speciation (e.g. Groot et al., 2008; Juárez et al., 2014).

This pest categorisation follows the taxonomy of Pogue (2011) and considers S. frugiperda as a single species with two strains.

3.1.2 Biology of the pest

Newly emerged adults appear from pupae in the soil shortly after dusk to feed and complete maturation. They do not mate on the first night. On subsequent nights, females sit at the top of a host plant and release a sex pheromone to attract a mate. Females mate once per night. Virgin females mate earlier in the night than females that have already mated (Sparks, 1979). Most oviposition occurs within 4 or 5 days although some females have been reported to oviposit for up to 17 days (Johnson, 1987). Adult females are relatively short-lived (13–19 days at 26.8°C) but highly fecund, with around 1,000 eggs being laid per female (Johnson, 1987).

Eggs are typically laid on the underside of leaves although at high population densities, almost any surface can be used. Eggs are laid in clusters of 100–300, sometimes in two layers. Clusters are protected with a covering of abdominal scales (CABI, 2017).

Depending on temperature, eggs usually take between 2 and 10 days to hatch. At mean temperatures of 21–27°C, eggs hatch in 2–4 days (Sparks, 1979).

After hatching, the first instars move to find a suitable feeding site on the plant where eggs were laid (Pannuti et al., 2015). The first and second instars feed together on young leaves and on the tender growing tips of hosts. Larvae can become cannibalistic at high larval densities when there is a shortage of host plant material to feed on (Andow et al., 2015). After about a week of development, third instar larvae disperse away from each other and continue to feed. In a trial examining larval dispersal of S. frugiperda, Pannuti et al. (2016) reported finding over 90% of recovered larvae within a 1.1 m radius of a maize plant 14 days after being infested with an egg mass. However, if larvae develop at high densities and when host resources are depleted, they will ‘march’ in search of food and move further and faster. There are five or six larval instars.

From studies examining larval development on different hosts, da Silva et al. (2017) found larvae developed 6–8 days faster feeding on maize, oats and wheat than on cotton. Development on soybean was about 5 days slower than on maize. Mature larvae burrow into the soil and create a pupal chamber 2–8 cm below the surface.

At 29°C, the pupal stage lasts around 7 days while at 15°C pupal development takes approximately 37 days (Sparks, 1979). Pupae developing during the winter in Florida did not complete development during a month where the minimum soil temperature was below 10°C for two or more days (Wood et al., 1979).

Overall, egg to adult development takes around 66 days at 18.3°C and 18 days at 35.0°C (Barfield et al., 1978). There is no significant difference between the development rates of males and females (Barfield et al., 1978). A threshold temperature of 10.9°C and 559 day-degrees above the threshold is required for development of the complete life cycle. The optimum temperature for development from egg to adult is 28°C (Ramirez Garcia et al., 1987).

All stages are usually killed by freezing temperatures (CABI, 2017).

In southern Florida, S. frugiperda can breed year round (Abrahams et al., 2017). There are continuous generations in Central and South America (Johnson, 1987) where there can be four to six generations per year (CABI, 2017).

3.1.3 Intraspecific diversity

As noted in Section 3.1.1, S. frugiperda is composed of two morphologically indistinguishable strains referred to as the maize and the rice strains. The two strains can be distinguished by strain-specific genetic markers (Lu et al., 1992; McMichael and Prowell, 1999). There are physiological and behavioural differences between strains, such as host plant preferences (Quisenberry and Whitford, 1988; Veenstra et al., 1995) and mating behaviour (Pashley et al., 1992). However, it is now recognised that host preference is not a reliable indicator of a strain (Juárez et al., 2012a, 2012b).

3.1.4 Detection and identification of the pest

3.2.1 Pest distribution outside the EU

S. frugiperda is native to tropical and subtropical regions of the Americas. It is established year round in northern Bolivia and from some parts of southern Brazil northwards through Central America and Mexico, the Caribbean and subtropical areas of southern Florida and Texas in the southern United States where winter temperatures rarely fall below 10°C (Sparks, 1979; Ashley et al., 1989; Nagoshi and Meagher, 2008). In mild winters, it can survive in Louisiana and Arizona (Wood et al., 1979). In summer, populations migrate into southern and northern temperate regions where it can become abundant in late summer and autumn.

In 2016, S. frugiperda was reported for the first time in Africa with outbreaks in Benin, Nigeria, Sao Tomé and Principe and Togo (Goergen et al., 2016; IITA, 2016) (Figure 1 and Table 2). How S. frugiperda arrived in Africa is uncertain, it may have entered via trade, or via weather systems associated with El Nino events of 2014-2016 (Wild, 2017). Subsequent reports confirm S. frugiperda has spread to several countries in west, central, east and southern Africa. News reports and media coverage indicate that S. frugiperda continues to spread in sub-Saharan Africa.

Wiltshire (1977) reports receiving a sample of male and female S. frugiperda from a colleague who collected specimens from the Jordan Valley in Israel in 1967. However, no other literature provided supporting evidence that S. frugiperda was established in Israel. We assume that any S. frugiperda found in Israel in 1967 were from a transient population that is no longer present.

3.2.2 Pest distribution in the EU

S. frugiperda was found on maize plants in Germany in August 1999. A total of 40 infected plants were found. Larvae were collected and destroyed (EPPO, 2000). Based on this incident, the EPPO Global Database and CABI (2017) currently records S. frugiperda as present in Germany based on information from the German NPPO in 2000. However, due to the eradication efforts at the time and the lack of subsequent reports, the Panel assumes that S. frugiperda in no longer present in Germany.

3.3.1 Council Directive 2000/29/EC

S. frugiperda is listed in Council Directive 2000/29/EC. Details are presented in Tables 3 and 4.

3.3.2 Legislation addressing plants and plant parts on which Spodoptera frugiperda is regulated

3.4.1 Host range

S. frugiperda is a polyphagous pest reported to infest 186 host plant species in North and Central America (Casmuz et al., 2010). It has a preference for wild and cultivated grasses, maize, rice, sorghum, millet and sugarcane (Poaceae). Other hosts from 27 families include Allium (Liliaceae), Brassica spp. (Brassicaceae), Capsicum and other Solanaceae including aubergines, potatoes and tomatoes, Cucumis (Cucurbitaceae), Gossypium (Malvaceae), Phaseolus (Fabaceae) and Ipomoea (Convolvulaceae) as well as various ornamental plants (chrysanthemums, carnations and Pelargonium) (Smith et al., 1997; CABI, 2017). In laboratory host preference studies examining larval feeding choices, maize and wheat were preferred above soybean and cotton (da Silva et al., 2017).

3.4.2 Entry

S. frugiperda is also a strong migrant flier. Having recently been introduced into Africa where it continues to spread, in future it may be able to enter the EU via summer migratory flight were it to establish in north Africa.

3.4.3 Establishment

Is the pest able to become established in the EU territory? (Yes or No)

Following the recent introduction of S. frugiperda into Africa, a preliminary examination of potential future distribution indicates that small parts of southern Europe provide suitable abiotic conditions for establishment (Abrahams et al., 2017). As a highly polyphagous pest, some of its hosts will be available, including maize and rice, in such regions. Biotic factors (host availability) and abiotic factors (summer climate) indicate that transient populations of S. frugiperda could occur in the summer further north in central and northern EU where maize is widely available.

3.4.3.2 Climatic conditions affecting establishment

S. frugiperda is native to tropical and subtropical regions of the Americas and has recently established in tropical and subtropical regions of Africa. It has no capacity to overwinter and all life stages are killed by freezing temperatures. In the USA, it is established in southern Texas and southern Florida where winter temperatures rarely fall below 10°C. Ramirez Garcia et al. (1987) report a life cycle is completed with 559 day-degrees above a threshold of 10.9°C. Based simply on this threshold and accumulated temperature, Figure 2 indicates that regions of the EU could be suitable for the development of S. frugiperda. Southern regions of Portugal, Spain, Italy, Greece and Cyprus are most suitable. More sophisticated modelling and mapping, e.g. taking into account factors such as consecutive days below 10°C or precipitation (amount and frequency), is beyond the scope of pest categorisation but would better inform decision makers as to the areas of the EU where abiotic factors most favour establishment.

3.4.4 Spread

As found in other species within the same genus, S. frugiperda has a notable dispersal capacity (Johnson, 1987). Adult annual migrations occurring in the summer result in the pest expanding from its endemic area in the warmer parts of the New World over more than 2,000 km across the entire US up to Canada in the north and reaching Argentina and Chile in the south (Luginbill, 1928; Sparks, 1979; Pair et al., 1986). Sparks (1979) and Johnson (1987) reproduce a map showing the typical northwards progression through time in the USA. Starting from southern Florida and Texas, the spring generation flies north, generally spreading up to approximately 300 miles before settling to reproduce the next generation. For example, in April and May, populations can be expected in Alabama and Georgia; in June and July later generations can be expected from South Carolina to Colorado and by late August subsequent generations can reach between North Dakota and Maine and into Canada. Prevailing winds and host availability influence the rate and direction of migrations (Hogg et al., 1982; Johnson, 1987).

More locally, larvae also disperse frequently from the original host plant, in part to compensate for the negative effects of overcrowding (Sparks, 1979; Pitre et al., 1983; Chapman et al., 1999). However, the contribution of such activities to overall spread is negligible compared to the movement by winged adults.

If S. frugiperda does establish in the Mediterranean region of the EU, there is potential for it to undertake spring and summer migrations, similar to those reported in the USA, so that there could be seasonal spread to more temperate areas of the EU. However, such populations would be transient and establishment limited by winter temperatures.

Given the natural dispersal ability of S. frugiperda, spread via plants for planting is not the main pathway for spread. S. frugiperda therefore fails to satisfy the important criterion that to be a RNQP, the main means of spread should be via plants for planting (Table 1).

3.5.1 Potential pest impacts

3.5.1.1 Direct impacts of the pest

S. frugiperda is a pest of several major crops in the Americas, particularly maize, sorghum, rice and sugar cane although many more crops and wild plants can be attacked.

In field trials, there was a significant loss in yield (17%), as measured by grain weight, when 20% of maize plants were infested with an egg mass (Cruz and Turpin, 1983). In trials in Mexico over a number of years, yield losses averaged 13%, maximum yield loss was 30% (Andrews, 1998). Pantoja et al. (1986) found yield reduction in rice was linearly related to larval density. Larval densities greater than 35 m⁻² resulted in yields significantly lower than in control plots.

Yield losses are due to larval feeding reducing photosynthetic capacity, destroying the growing tip of crops or if later instar larvae cut through the stems of young plants. In a laboratory trial, the first three instars were reported to eat less than 2% of all the foliage consumed during development, while the final and largest instar consumed over 75% of the total (Sparks, 1979).

In the USA, outbreaks occur in warmer years when adults spread north earlier than normal and populations build up faster and affect less mature plants, causing greater yield losses and increasing expenditure on control. Outbreaks occurred irregularly in the USA during the 19th and 20th Centuries. In 1977 costs were estimated to be almost $300 million (Johnson, 1987) with losses in Georgia estimated at around $138 million (Sparks, 1979).

S. frugiperda is described by the USDA as ‘economically important’ (Ellis, 2005) and is an important pest in nine south-eastern states of the USA where annual average yield loss between 1975 and 1983 was $ 60 million (Sparks, 1986).

S. frugiperda is considered the most important pest of maize in Brazil, estimated to cause more than US $400 million damage annually (IITA, 2016). The FAO estimates Brazil spends US $600 million annually controlling infestations of S. frugiperda (Wild, 2017).

Following its introduction into Africa, S. frugiperda has been reported damaging maize (Goergen et al., 2016). In Kenya, S. frugiperda is also attacking cotton, sugar cane, banana and vegetables. Across the infested area, rice and sorghum are important food crops that are also threatened (Abrahams et al., 2017). At an FAO organised meeting to discuss plans to respond to S. frugiperda in Africa, it was reported that 290,000 ha of crops had been destroyed by larvae in four countries although this was probably an underestimate (Wild, 2017).

Were S. frugiperda to establish in the EU, it could reduce yields on crops particularly maize, rice and sorghum during outbreak years. However, the areas most suitable for the pest to establish occur in the far south of the EU where these crops, other than rice, are less intensively planted. Figure 3 shows a preliminary estimate of the annual number of generations that might develop in the EU. Four generations might be possible in the far south of Spain, Portugal, Italy and Greece and in Cyprus.

Other major crops grown in the EU such as wheat, onions, potatoes, strawberries, sugarbeet and Citrus are also hosts to S. frugiperda although no yield loss reports were obtained during the pest categorisation. There is therefore uncertainty as to the likely consequences to these crops were S. frugiperda to establish in the EU.

3.6.1 Biological or technical factors limiting the feasibility and effectiveness of measures to prevent the entry, establishment and spread of the pest

• Possible seasonal natural migration of adult moths northwards from Africa into the EU; spread can exceed 2,000 km during the summer.
• Cultivated preferred hosts such as maize, rice and cotton occur in Mediterranean EU countries where the climate could support establishment.
• Polyphagy, 186 hosts, including non-cultivated species, have been described for S. frugiperda (Casmuz et al., 2010)
• In the Americas, transgenic maize expressing Bacillus thuringiensis insecticidal proteins is widely used to control a range of pests, including S. frugiperda. However, although the use of Bt maize is allowed in the EU, there is a reluctance and only five EU MS (Spain, Portugal, the Czech Republic, Slovakia and Romania, in decreasing order of ha of Bt-maize cultivated) actually grew this type of crop in 2015 (http://isaaa.org/resources/publications/briefs/51/executivesummary/default.asp).
• S. frugiperda has developed resistance against at least 24 different active substances (University of Michigan, 2017) including some B. thuringiensis insecticidal proteins used in transgenic maize crops (Aguirre et al., 2016; Abrahams et al., 2017).

3.6.2 Biological or technical factors limiting the ability to prevent the presence of the pest on plants for planting

• Resistance to insecticides (as above).

3.6.3 Control methods

• Chemical control (Dequech et al., 2013; Abrahams et al., 2017)
• Biological control:
  • –Effective natural enemies occur in the Americas and could be considered as candidates for Classical Biological Control (Abrahams et al., 2017)
  • –Different entomopathogens have been screened and could be effectively used as bioinsecticides to control this pest (Barrera et al., 2011; Behle and Popham, 2012)
• Biotechnological control: GMOs,, use of semiochemicals (pheromone)
• Area-wide IPM to control resident populations in overwintering sites (Meagher & Nagoshi, 2004)
• Cultural control: could the push-and-pull method currently practiced in Africa against maize borers by small farmers be effective against S. frugiperda?

It should be noted that European maize growers currently manage lepidopteran pests related to S. frugiperda; they are Sesamia nonagriodes (the Mediterranean corn borer) and Ostrinia nubilalis (European corn borer). What effect the management practices used against these pests may have on S. frugiperda is unknown.