Thaumatotibia leucotreta
(false codling moth (FCM))

T. leucotreta is endemic to sub-Saharan Africa and has shown itself to be an ineffective invader. It has only successfully established in two regions where it is not indigenous; these are the Western Cape of South Africa (Giliomee and Riedl, 1998; Hofmeyr et al., 2015) and Israel (Wysoki, 1986). Further confirming its poor dispersal and colonisation ability is the fact that it has not spread further in the Middle East than Israel, despite being established there for about 35 years. Furthermore, generally being a solitary infestor of fruit (unlike fruit flies) (Grout and Moore, 2015; Hatting et al., 2019), with the possible exception of pomegranates, mate finding and the consequent probability of establishment in a new environment is dramatically reduced.

T. leucotreta has occasionally been recorded in Europe. However, these have been isolated recordings, where it has been imported with produce from Africa, rather than from established populations (Bradley et al., 1979; Karvonen, 1983; Knill-Jones, 1994; Langmaid, 1996; Huisman and Koster, 2000; Svensson, 2002). In 2009, an incursion of T. leucotreta was detected in the Netherlands on glasshouse Capsicum chinense, but was subsequently eradicated (EPPO, 2010; Potting and van der Straten, 2011).

Following the detection of a single adult male in a trap in Ventura County, California, USA, in 2008 (Gilligan et al., 2011), APHIS and the California Department of Food and Agriculture (CDFA) conducted extensive surveys for T. leucotreta throughout the state. There have been no further detections of the pest in California, and the 2008 detection is considered an isolated regulatory incident. T. leucotreta is listed as a quarantine pest in the USA (NAPPO, 2016), the EU (European Union, 2017) and several other countries.

T. leucotreta is extremely polyphagous, there being in excess of 70 food plants recorded. However, the validity of many of the listed host plants has been questioned or even refuted (EPPO, 2013; Moore et al., 2015b).

Schwartz (1981) used 10 references, dating from 1901 to 1976 in compiling a list of 35 host plants, of which 21 were cultivated. Venette et al. (2003) used 15 references dating from 1972 to 2003 in compiling their list of 70 host plants of T. leucotreta. EPPO (2013) used some of the same and several other references, dating from 1958 to 2010 in compiling a list of 107 previously listed hosts. However, they questioned the validity of several of these and even outright refuted 36 of the listed host species (Moore et al., 2015b). This was based on a thorough investigation of the literature and the conclusion that reporting was often ambiguous or there was no original source of substantiating data. Most recently, Brown et al. (2014) has significantly added to the list of hosts, particularly wild indigenous and naturalised hosts in East Africa (Kenya), including some which are cultivated. It should also be noted that there are differences in host status of certain crops in different regions. For example, maize is recorded as an important host in West Africa (Schulthess et al., 1991), cotton as a notable host in East Africa (Reed, 1974) and Ricinus as a conspicuous host in Israel, whereas in southern Africa, infestation on all of these hosts is considered as extremely rare.

The female moth lays 100-400 or even more eggs at night, usually singly on the bolls, fruit or nuts of the plant. On citrus the young larva mines just beneath the surface, or bores into the pith causing premature ripening of the fruit. On cotton it first mines the boll wall, but later transfers to the seeds.

When full grown the larva descends to the ground on a silken thread and spins a tough silken cocoon in the top few millimetres of soil or amongst debris (Love et al., 2019). The development time for each stage varies considerably with temperature; details are given by Daiber (1980) who states that in South Africa five generations per year could be achieved by the moth. There is no diapause (Terblanche et al., 2014).

The adult is nocturnal and although found to be attracted to light in a laboratory set up, this has not been the case in the field (Gunn, 1921; Catling and Aschenborn, 1978). The mating behaviour is highly developed and relates to three androconial areas on the male (Zagatti and Castel, 1987).

These will vary according to the crop affected. On oranges look for a yellow patch on the skin of green fruit and a brown patch on the skin, usually with evidence of a hole bored in the centre, sometimes with dark brown frass exuding.

In West Africa, T. leucotreta is often found in conjunction with the pyralid moth Mussidia nigrevenella. Differences between the larvae are given by Silvie (1990) and Moyal and Tran (1989).

In citrus in southern Africa, the only lepidopteran larva with which T. leucotreta could be confused is the carob moth, Ectomyelois ceratoniae, but fairly straightforward diagnostic criteria (e.g. Timm et al. (2007, 2008) and Rentel (2013)) enable accurate differentiation. In macadamias, pecans and litchis, other species, such as Cryptophlebia peltastica, Thaumatotibia batrachopa and E. ceratoniae can occur, but can be differentiated according to Timm et al. (2007, 2008) and Rentel (2013).

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Introduction

There is currently a wide range of effective control options available (Moore and Hattingh, 2016; Malan et al., 2018). However, as T. leucotreta is indigenous wherever it occurs, with the exception of Israel, the occurrence of alternative wild hosts can lead to reinfestation, if growing in close proximity to the crop. However, T. leucotreta is a poor disperser and coloniser (Newton, 1998; Stotter et al., 2014) so this reinfestation would be a slow process.  Additionally, a plethora of natural enemies would maintain suppression of the pest, if undisrupted within an IPM approach.

Monitoring

T. leucotreta is monitored using a combination of pheromone traps and fruit infestation (Moore et al., 2008). Amongst others, Newton et al. (1993) identified the female pheromone and Hofmeyr and Burger (1995) developed the original pheromone dispenser. However, due to the phytosanitary status of T. leucotreta for many export markets, traps are no longer used to determine whether intervention is necessary, but rather to assist with accurate timing and prioritisation of treatments (Moore et al., 2008).

Cultural Control

Reed (1974) and Byaruhanga and De Lima (1977) showed that late-sown crops of cotton in Uganda were worst affected, but the difference was not great. As T. leucotreta is primarily a fruit feeder, it is suggested by Glas (1991) that crops of cotton grown close to fruit trees may be less affected. Ullyett and Bishop (1938) found that weekly sanitation in citrus orchards (picking up and destruction of fallen fruit) reduced fruit loss from 6.1 to 3.3%. Stofberg (1954) found that a programme of regular sanitation could save between 24 and 60 fruit per tree from T. leucotreta infestation. He concluded that at that time, the cost of twice-weekly sanitation would be justified if T. leucotreta infestation was reduced by half. Moore and Kirkman (2008) showed that weekly orchard sanitation from December to June removed an average of 75% of T. leucotreta larvae infesting fruit. Orchard sanitation is considered as the backbone for effective control of T. leucotreta.

Biological Control

Parasitoids of T. leucotreta have been identified, and mass release of Trichogrammoide acryptophlebiae has been shown to be effective (Newton and Odendaal, 1990). Parasitoids are currently commercially available for augmentation (Malan et al., 2018) and have been shown to reduce T. leucotreta infestation by up to 60% (Newton and Odendaal, 1990; Moore and Hattingh, 2016).

Cryptophlebia leucotreta granulovirus (CrleGV) has been used commercially for more than 15 years, reducing T. leucotreta by up to more than 90%, with a residual efficacy from one spray of up to 17 weeks (Moore et al., 2015a). Currently, there are three commercially available CrleGV products on the market (Hatting et al., 2019).

Entomopathogenic fungi, Beauveria bassiana and Metarhizium anisopliae, isolated from citrus orchards (Goble et al., 2010, 2011; Coombes et al., 2013, 2015) reduced T. leucotreta infestation of citrus fruit by over 80% during a full season, from a single spring application to the soil (Moore et al., 2013; Coombes et al., 2016). However, these isolates are still to be commercially developed, and currently, the only EPF registered for control of T. leucotreta in southern Africa are applied to the tree for control of the egg and neonate larval stages.

An EPN product, with its active ingredient Heterorhabditis bacteriophora, is registered for use against the soil-dwelling life stage of T. leucotreta in South Africa (Malan et al., 2018). Application of H. bacteriophora to a citrus orchard floor, reduced T. leucotreta infestation of fruit by up to 81% (Moore et al., 2013).

Sterile Insect Technique

The Sterile Insect Technique (SIT), as a stand-alone treatment in a semi-commercial trial, reduced T. leucotreta infestation in 35 ha of Navel orange orchards by 95.2%, relative to an untreated control orchard (Hofmeyr et al., 2016a). These initial findings led to commercial implementation for control of T. leucotreta within an integrated programme in citrus, since 2007. The programme is proving extremely effective (Hofmeyr et al., 2015), having reduced moth catches by 99%, fruit infestation by 96% and export rejections by 89% since the inception of the programme (Barnes et al., 2015). After orchard sanitation, area-wide techniques, such as SIT and mating disruption, are considered as the most important control tactics for T. leucotreta.

Chemical Control

Chemical control of T. leucotreta has been shown to be effective. In field trials two synthetic pyrethroids, applied 2-3 months before harvest, reduced fruit drop by an average of 90% (Moore and Hattingh, 2016). Field trials conducted by Newton (1987) showed that a single application of the insect growth regulators, triflumuron or teflubenzuron, reduced fruit loss by up to 86%. Although T. leucotreta insecticide resistance has been reported for the older chemical control options (Hofmeyr and Pringle, 1998), Moore et al. (2015a) showed that the more recently registered chemicals, such as methoxyfenozide and spinetoram are also effective in controlling T. leucotreta infestation. Although chemical control is effective and important, there are sufficient effective non-chemical treatments available in order to not be reliant upon chemical control for T. leucotreta management.

Pheromonal Control

Field trials conducted with mating disruption in Navel orange orchards, reduced T. leucotreta infestation by 55 to 75% (Hofmeyr and Hofmeyr, 2002; Moore and Hattingh, 2012). More importantly, these reductions were 86 and 95%, respectively, in later evaluations shortly before harvest. Currently, there are four mating disruption products and one attract and kill product that are commercially available for use against T. leucotreta (Malan et al., 2018).

Postharvest Control

Cottier (1952) demonstrated the efficacy of T. leucotreta postharvest cold treatment by shipping infested fruit from South Africa to New Zealand at a pulp temperature of -0.55°C for 21 days, with no survival of any larvae and eggs. Myburgh (1963, 1965), conducted further trials and concluded that 21 to 22 days at -0.55°C would provide at least a Probit 9 level of control. More recently, Moore et al. (2017) demonstrated that the following treatments caused mortality at or in excess of the probit 9 level: 16 d at or below -0.1°C, 18 d at or below -0.3°C, 20 d at or below -0.3°C and 19 d at or below 1.2°C. Ware and du Toit (2011, 2016, 2018), respectively, demonstrated Probit 9 efficacy in grapes at 2°C for 22 days; demonstrated Probit 8.7 efficacy in avocadoes at -0.6°C for 18 d and at 0.8°C for 20 d; and recorded only one survivor out of 28,380 larvae treated in avocadoes at 2°C pulp temperature for 20 days. Some countries to which South Africa exports fruit require a disinfestation cold treatment as a phytosanitary risk mitigation measure for T. leucotreta (South African Department of Agriculture Forestry and Fisheries, 2015).

Ionizing radiation with 100 Gy, as a postharvest phytosanitary disinfestation treatment for T. leucotreta larvae and eggs, was effective at the Probit 9 level (Hofmeyr et al., 2016b, 2016c). A combination of 60 Gy followed by 16 days at 2.5°C was also effective at the Probit 9 level (Hofmeyr et al., 2016d, 2016e).

Systems Approach Control

Moore et al. (2016) and Hattingh et al. (2020) developed a systems approach consisting of three measures: 1) preharvest controls and measurements and postpicking sampling, inspection, and packinghouse procedures; 2) postpacking sampling and inspection; and 3) shipping conditions. They demonstrated that the maximum potential proportion of fruit that may be infested with live T. leucotreta after application of the systems approach is no greater than the proportion of fruit that may be infested after application of a Probit 9 efficacy postharvest disinfestation treatment to fruit with a 2% pretreatment infestation. This system has been used for export of citrus from South Africa to the EU, as an alternative to a stand-alone cold treatment.

21/05/20 Review by:

Elma Carstens, Citrus Research Institute, Nelspruit, South Africa

Sean Moore, Citrus Research Institute, Nelspruit, South Africa