HL01107 - Biological, semiochemical and selective chemical management methods for insecticide resistant western flower thrips on protected strawberry

Aim of Initiative

The aim of the proposed project is to develop a comprehensive range of new effective methods for managing insecticide resistant western flower thrips (WFT) on tunnel-grown strawberry in the UK. The methods will include an improved semiochemical monitoring trap with attendant damage thresholds, a computer-based population and risk forecasting model, new selective pesticide treatments, new biopesticides and novel, more cost-effective strategies for using existing predators. These components will be integrated into a comprehensive management strategy for the pest which will be tested on a commercial scale in the later stages of the project.

Commercial and Technical Background

Western flower thrips, Frankliniellaoccidentalis, is highly resistant to many pesticides. Spinosad (Tracer) became available for use on protected strawberries in 2005 and was the most effective pesticide against the pest until 2008, when a population on everbearer strawberry was confirmed to be resistant. Since then, severe resistance to spinosad has been confirmed on several other UKeverbearer crops. Recent resistance tests have shown that >12 fold resistance to spinosad and other pesticides. Several growers have failed to control the pest using multiple sprays of the full range of approved plant protection products. In short, the pest has become much more difficult to control. There are no fall-back treatments if biocontrol programmes fail. Serious outbreaks in warmer weather conditions that favour the pest in mid and late summer caused serious crop losses and several fields had to be abandoned and prematurely grubbed on farms in southern England and the Midlands in 2009.

The pest feeds in strawberry flowers and on young developing fruitlets, sucking sap from surface cells and causing the fruitlets to have a bronze, unsightly appearance. Such fruit is unmarketable and even slight damage around one or two seeds can cause fruit to be downgraded or rejected. Many growers make routine introductions of the predatory mite Amblyseiuscucumeris in spring against this and other pests. However, this strategy is inadequate when high populations of thrips develop early. A. cucumeris feeds only on young thrips larvae and can become overwhelmed by large influxes of WFT adults e.g. from infested growing media held over from the previous season or from adjacent infested crops. Other available/recommended biocontrol agents are either costly (e.g. Oriuspredatory bugs), are of doubtful efficacy in the low moisture content soils of everbearer beds (e.g. the predatory mite Hypoaspis miles, entomopathogenic nematodes) or cannot currently be introduced into polythene tunnels because they are not native (e.g. Amblyseiusswirskii).

HDC-funded screening trials of a wide range of existing and novel insecticides in 2008 and 2009 failed to identify any suitable adequately effective alternative insecticides. Though a liquid methiocarb formulation gave good results, it is unlikely to be registered for use on strawberry in the UK because of its toxicological and environmental hazards.

Strawberry production in the UK is intensive and the crop is of high value (£212M in 2007), the UK industry being amongst the most effective in Europe. The majority (>80%) of strawberries sold by multiple retailers are grown under protection to secure continuity of supply and quality of production. Late season production with everbearer varieties has expanded so that the market is supplied for a greater proportion of the season.

The average everbearer strawberry crop yields 20,000 kg of class 1 fruit per ha over one season with a current value of £2.70 per kg (i.e. £54,000 per ha). On some farms during 2009, WFT damage to everbearer fruit has been so severe following failure of spinosad to control the pest that total crop loss has occurred for the latter third of the season, i.e. a loss of c. £18,000 per ha. More typically, on some farms 20% of the fruit has been downgraded to class 2 for half of the picking season. The value of class 2 fruit is less than £1.50 per kg. In this case, WFT has caused estimated financial losses of approximately £3,000 per ha per season. There is great concern that the losses will become more widespread in future years if the spread of spinosad resistant strains of WFT occurs. The cost of this proposed research is thus small in relation to the annual losses being incurred by the UK strawberry industry.

The Problem/Opportunity

The widespread occurrence of resistant strains of western flower thrips that cannot be controlled with insecticides and the lack of adequate, reliable and cost effective biocontrol agents and/or adequate knowledge on how to use existing biocontrol agents in tunnel-grown everbearers means that the pest poses an immediate and serious threat to the economic viability of strawberry production in the UK. Substantial areas of intensive production have been abandoned resulting in serious financial losses.

There is opportunity to develop new solutions for this pest that do not rely on pesticides to which resistance rapidly develops. An intensive research effort is urgently needed to develop a range of new methods for managing the pest, including a new specific semiochemical lure and trap for monitoring the pest, a risk prediction model, new biopesticides and improved ways of using existing biocontrol agents. Further research is needed to integrate these methods into a joined-up IPM programme for the pest which is suitable for use by growers.

Scientific Background and Approaches

Monitoring/semiochemicals

  • WFT is strongly attracted to particular colours, such as blue and yellow, which are used on sticky traps for monitoring in greenhouses (Vernon and Gillespie, 1990; Steiner and Goodwin, 2005a).
  • Two components of the male-produced aggregation pheromone of WFT have been identified as (R)-lavandulyl acetate and neryl (S)-2-methylbutanoate (Kirk and Hamilton, 2004; Hamilton et al., 2005). The latter attracts both females and males (Hamilton et al., 2005). It is used commercially (Thripline) on blue or yellow sticky traps for monitoring WFT in greenhouses (Gómez et al., 2006) and recent trials have shown that it is also effective outdoors in orchards (Broughton, 2009). The pheromone does not attract other thrips species.
  • A range of pyridine compounds, including a commercial lure for WFT (Lurem), based on plant attractants, increases trap catches, but they are not specific for WFT (van Tol et al., 2007).
  • Further increases in trap catches should be possible by combining attractants, optimising doses and ratios, and modifying the dispenser. Traps are likely to be at least as effective outdoors or in Spanish tunnels as in glasshouses, as has been found with plant attractants for other species of thrips (Teulon et al., 1993).
  • Sticky traps outdoors or in tunnels are liable to become congested with insects other than WFT, so it will be necessary to design a monitoring trap that is highly attractive to WFT while not attracting other insects and/or excluding them.
  • Action thresholds in terms of thrips per flower have been established for glasshouse strawberry crops in Australia, which vary according to temperature, humidity and stage of the crop (Steiner and Goodwin, 2005b). Thresholds in terms of numbers of WFT per flower, which correlated with consequent fruit damage, have been established in field-grown strawberries in Israel (Coll et al., 2007).
  • Yellow sticky traps in glasshouse strawberry crops have shown a correlation between trap catch and density of WFT on the crop (Steiner and Goodwin, 2005a). An action threshold based on the sex ratio on the traps was determined, but this is not practical for grower use in the UK.
  • Results of field trials on commercial everbearer crops in the UK in HDC-funded project SF 80 demonstrated that different strawberry cultivars may vary in their susceptibility to fruit damage (Bennison and Fitzgerald 2007, 2008 & 2009). Thus damage thresholds may vary between strawberry cultivars.

Modelling population development

  • The population growth of WFT depends mainly on temperature and host plant. Most WFT developmental data have been obtained on cucumber and chrysanthemum in glasshouse crops (Gaum et al., 1994; Nothnagl et al., 2007; Nothnagl et al., 2008; Rhainds et al., 2007; Wang and Shipp, 2001). Development is fastest at 28-30°C. Above 35°C and below 10°C WFT development effectively stops. At higher temperatures mortality rises rapidly and lifespan declines sharply; mortality does not increase appreciably at low temperatures (>10°C).
  • At optimum temperatures, generation time can be as short as 11 days on chrysanthemum, compared to 39 days at 15°C (Robb, 1989). In the early season in the UK, crop canopy temperatures usually fluctuate greatly in the range of 5-30°C under Spanish tunnels (Bennison and Fitzgerald, 2009).
  • Apart from temperature, several other factors also affect WFT development, includingrelative humidity, the species of host plant and types of host tissues (Chaisuekul and Riley, 2005; Gaumet al., 1994; Ishida et al., 2003; Katayama, 1997; Trichilo and Leigh, 1988).
  • The precise relationship of WFT development with temperature is not known on strawberry, especially for temperature < 16°C, and observations have also suggested that WFT development differs greatly on leaves and flowers. Most of the population, however, is likely to be on flowers and fruit when they are available. Depending on temperatures, many generations of WFT can develop within a season on ever-bearer strawberry.
  • Predicting WFT population development may assist growers in controlling WFT by allowing accurate timing of biological control agents/pesticides for maximum control, and assisting in interpreting trap catches.

Predators

  • UK growers of glasshouse strawberries have successfully controlled WFT by using the predatory mite Neoseiulus (Amblyseius) cucumeris. However, use of A. cucumerishas proved unreliable in everbearer strawberries grown outdoors or in Spanish tunnels.
  • Everbearer strawberries suffer particularly high losses from WFT damage to fruit due to the long flowering and fruiting season.
  • In SF 80 (Bennisonand Fitzgerald, 2009) it was shown that:
  • WFT overwinter in everbearer fields, so WFT populations and fruit damage can be particularly high where plants or beds are kept from one season to the next.
  • WFT are active from March onwards, much earlier than most growers consider releasing A. cucumeris for WFT control. Many growers are likely to be releasing too few predators, too late. In addition, they often use pesticides against other pests that have adverse effects on the predator.
  • As A. cucumeris only feed on first stage WFT larvae, in order to stand a chance of successfully controlling WFT it needs to be established in the crop before overwintered adult thrips become active and begin to reproduce. However, the mites need a minimum temperature of 8°C to be able to reproduce.
  • In a ‘proof of principle’ experiment with high release rates, A. cucumerisestablished in everbearer strawberries when released in May from slow-release sachets. These releases led to lower WFT numbers and less damaged fruit than on untreated plants. However, control of WFT was only maintained until early July when spinosad (Tracer) was applied to reduce thrips numbers. With the subsequent development of spinosad resistance in everbearer crops, development of more effective biological control strategies is urgently needed.
  • Strategies for cost-effective releases of this predator need fine-tuning and the concept of early releases more rigorously tested.
  • Since A. cucumeris only consumes first instarWFT larvae, where WFT pressure is high, additional biocontrols are needed to control other WFT life stages. Currently the most promising candidate for use in combination with A. cucumerisis the predatory bug Oriuslaevigatus. This predator eats both thrips adults and larvae and also pollen. However it is considered by growers to be expensive, and is also very susceptible to some pesticides currently used to control other strawberry pests. Combinations of releases of A. cucumeris and Orius spp. have not been tested for their effectiveness in UKeverbearer strawberry crops. However, this combination of predators has given good results in tunnel-grown strawberry crops in France (Clare Sampson, personal communication).
  • The use of flowering trap/refuge/’banker’ plants may help to improve the establishment and augmentation of O. laevigatus. This novel technique has not been assessed in strawberry plantations.
  • The use of banker plants in strawberry crops might also attract other naturally-occurring predators, which could be important in a biological approach to pest control. The use of a molecular technique to identify naturally-occurring predators that have consumed WFT may give pointers to novel biocontrol agents for this pest.

Biopesticides

  • Fungi are important natural enemies of insects and can be used as an alternative insect control measure as they have contact action, work quickly, and can be applied to the crop using conventional spray apparatus.
  • Frankliniellaoccidentalis is susceptible to at least seven species of entomopathogenic fungi: Conidioboluscoronatus, Beauveriabassiana, Metarhizium anisopliae, Neozygitesparvispora, Paecilomycesfarinosus, Paecilomycesfumosoroseus and Verticilliumlecanii (Butt andBrownbridge, 1997 and references therein).
  • Three commercial fungal biopesticides are reported to have activity against F. occidentalis(Shah and Goettel, 1999). Mycotal (Koppert BV, Netherlands), which is based on Lecanicilliummuscariumand is registered in the UK (Helyer et al., 1992), Naturalis-L (Intrachem, Italy) which is based on B. bassiana and recently approved in the UK (Wright and Kennedy, 1996) and a second B. bassiana-based product, BotaniGard WP (Emerald Bio, USA) which is sold in the USA and mainland Europe for the management of glasshouse pests, including thrips (Bradley et al., 1998).
  • In studies at HRI (HDC funded research PC 129), both Naturalis-L and BotaniGard were evaluated against F. occidentalis on glasshouse grown cucumber crops (Jacobson et al., 2001). Two high volume sprays of Naturalis-L, applied with a six day interval, reduced numbers of immature F. occidentalis by 75% compared with an untreated control during the three weeks following the first application. Glasshouse populations of F. occidentalis were also reduced by 65 – 87% with three consecutive high volume sprays or low volume mist applications of Naturalis-L or BotaniGard WP, applied at six day intervals. Subsequent Defra funded research (HH3102TPC) showed that both the strains of Beauveria used in Naturalis-L and BotaniGard WP were significantly less effective against larvae than adult thrips (Bennisonet al., 2006). There is therefore potential to select new fungal strains with improved activity against larvae.
  • Entomopathogenic fungi infect their hosts using spores that germinate on and penetrate the insect cuticle. This is a critical phase in the infection cycle because the spores are exposed to potentially detrimental environmental conditions, of which the most important is low relative humidity. It is important therefore to know the time required for infection so that the most appropriate application schedule can be used e.g. spraying fungi at night when humidity is higher.
  • Defra funded research (HH3102TPC) showed that 95-98% of WFT larvae dropped to the ground to pupate which offers the opportunity to use fungal biopesticidesagainst the ground-dwelling stages. Both Naturalis-L and BotaniGard WP were not effective against pupae in this study (Bennison et al., 2006), however other fungus species or isolates could be more active against pupae and there is evidence that strains of B. bassiana, M. anisopliae, and V. lecanii can suppress F. occidentalis pupae in soil or potting media (Brownbridge et al., 1994; Vestergaard et al., 1995, Ansari et al., 2008).
  • Currently approvedentomopathogenic fungi (Naturalis-L and Mycotal) need to be tested as foliar sprays on strawberries.

Pesticides

  • WFT readily develops resistant strains to insecticides. Populations with high levels of resistance to the complete range of insecticides approved on strawberry have recently become widespread in commercial strawberry crops in the UK. Recent resistance tests have shown that >12 fold resistance to spinosad, one of the key insecticides relied on by growers, has developed and several growers have failed to control the pest with multiple sprays of the full range of approved plant protection products. The pest has become much more difficult to control and there is now no fall-back to support biocontrol programmes.
  • Several insecticides approved for control of pests on strawberry are considered to have some activity against WFT. These include Dynamec, EradicoatandMajestik (natural plant extracts) and Tracer (spinosad). Tracer was considered to be the most effective of these but poor results were obtained even after 4 applications (the statutory maximum) in several crops in 2008 and 2009 due to the development of resistance, which now appears to be widespread and gaining momentum.
  • HDC funded project SF60 in 2004 evaluated IPM-compatible insecticides and potential biocontrol agents for thrips control. Eight insecticides were tested for their efficacy against WFT. Tracer was the only insecticide which was effective in laboratory bioassays giving 88% mortality after 48 hours. Dynamec, Calypso (thiacloprid), Talstar, Trigard, Majestik and Masai (tebufenpyrad) were not effective (see SF60, 2004). However, this laboratory test only evaluated the contact mode of action of the products tested.
  • In 2008 and 2009, two replicated experiments were conducted in heavily infested protected strawberry plantations in Kent to test products for the control of resistant strains of WFT in strawberry flowers. Products tested (two sprays at an interval of 7 days) were Dynamec, Calypso, Tracer, Break-Thru S 240 (silicone adjuvant), Mesurol (methiocarb), Pyrethrum 5EC (pyrethrum), Teppeki (flonicamid), Dantop (clothianidin), Nemolt (teflubenzuron), Gazelle (acetamiprid), Movento (spirotetramat), Neemazal (Neem extract), and a novel coded product HDCI1. The biopesticideNaturalis-L (Beauveriabassiana) was also included.
  • Mesurol was consistently the most effective product but Gazelle, Movento and Naturalis also showed activity. The efficacy of Mesurol was enhanced by the use of a silicone-based adjuvant but the use of silicone based adjuvants has not been investigated with other products.
  • Mesurol is unlikely to receive approval in the UK and furthermore it is incompatible with biological control agents e.g. it is harmful to Phytoseiuluspersimilis, Oriusspp. and Amblyseiuscucumeris, with a persistent effect for up to 8 weeks.
  • Further work is needed to explore the use of products showing activity alone, in mixtures and in admixture with adjuvants. Further novel active ingredients also need to be evaluated (at least one ‘coded’ compound with possible activity has not yet been evaluated).

Key requirements for pesticides for WFT on strawberries are safety to bees and pollinating insects, safety to the crop, safety to beneficial insects and biocontrol agents as well as likelihood of future registration on strawberries