Crop Protection 42 (2012) 156e163

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Crop Protection

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Evaluation of monitoring methods for and the effect of trap colour and semiochemicals on sticky trap capture of thrips (Thysanoptera) and beneficial (Syrphidae, ) in deciduous fruit trees in Western Australia

Sonya Broughton*, Jessica Harrison

Department of Agriculture and Food Western Australia, 3 Baron-Hay Court, South Perth, WA 6151, Australia article info abstract

Article history: Western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), plague thrips Received 3 May 2012 (Thrips imaginis Bagnall), and onion thrips (Thrips tabaci Lindeman) are pests of deciduous fruit trees in Accepted 7 May 2012 Australia. Yellow sticky traps and tapping buds and flowers for thrips are currently recommended for monitoring, but it is not known whether one method is more efficient than the other, or if selectivity Keywords: Ò could be optimised by trap colour, or addition of semiochemicals Thriplineams or Lurem-TR lures to traps. Frankliniella occidentalis The number and species of thrips caught by trapping and tapping of flowers and leaves, on different trap Thrips imaginis colours (black, blue, green, red, yellow, white), including a control (clear) and thrips semiochemicals, Thrips tabaci Semiochemicals were evaluated in a series of trials in commercial deciduous fruit orchards in the Perth Hills, Western 2 ¼ Lurem-TR Australia. There was poor correlation between thrips caught on traps and tapping samples (R 0.00 Ò e Thriplineams 0.05), with tapping less likely to trigger the action threshold and yielding less than 1% of the Beneficial insects number of thrips caught on sticky traps. More thrips (F. occidentalis, T. imaginis and T. tabaci) were caught on blue, yellow and white bases, than on clear, red, green or black bases. On commercially available sticky traps, seven times more F. occidentalis were caught on ‘Seabright blue’ traps than yellow. The addition of semiochemicals increased capture of F. occidentalis by three times on baited compared to unbaited traps, Ò on yellow and ‘Seabright’ blue traps. Thriplineams attracted F. occidentalis, but had no effect on the capture of T. imaginis or T. tabaci, whilst Lurem-TR attracted more F. occidentalis and also increased the capture of T. imaginis. More beneficial insects including brown lacewings ( (Walker)) and hoverflies (Melangyna viridiceps (Macquart)) were caught on blue trap bases (1.6 times more) than other Ò trap base colours. No beneficial insects were present during the Thriplineams experiment, whilst Lurem- TR increased trap capture of brown lacewings by 1.3 times. A monitoring system incorporating blue Ò sticky traps in conjunction with Thriplineams would be more selective at detecting and monitoring F. occidentalis in deciduous fruit in Australia. Crown Copyright Ó 2012 Published by Elsevier Ltd. All rights reserved.

1. Introduction by feeding on, and scarring, the ovaries of peaches (Prunus persicae (L.) Batsch, Rosaceae), plums (Prunus domestica L., Rosaceae) and Thysanoptera (thrips) are key pests of deciduous fruits in nectarines (Prunus persica variety nectarine, Rosaceae) from late Australia, causing damage at flowering or fruit set (early season bloom through to petal/shuck fall (Brough et al., 1994). Onion damage), or as fruits mature (late season damage) (Hardy et al., (Thrips tabaci (Lindeman)) and tomato thrips (Frankliniella schultzei 2005), resulting in reduction in market value of crops. Native pla- (Trybom)) have also been recorded as sporadic pests of deciduous gue thrips (Thrips imaginis (Bagnall)) were first recorded as a pest of fruits (Steiner, 2008), attacking fruit 2e3 weeks before harvest. apples in the 1930s. Adult T. imaginis reduce pollination by feeding Silvering or whitening of the skin is caused by adults and larvae on the flower parts and fruit stalks (Evans, 1932; Brough et al., feeding on the fruit surface, with damage more apparent in pro- 1994). The larvae cause scarring, surface russeting and corkiness tected areas where thrips shelter. In the last decade, economic losses due to thrips damage has increased and is attributable to the spread of western flower thrips * Corresponding author. Tel.: þ61 08 9368 3271; fax: þ61 08 9474 2840. (Frankliniella occidentalis (Pergande)) into fruit growing areas E-mail address: [email protected] (S. Broughton). (Broughton et al., 2011). First detected in Western Australia in 1993

0261-2194/$ e see front matter Crown Copyright Ó 2012 Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.cropro.2012.05.004 S. Broughton, J. Harrison / Crop Protection 42 (2012) 156e163 157

(Malipatil et al., 1993), F. occidentalis is now regarded to be a serious water traps in wheat (Bowie et al., 1999). However, Chen et al. regional issue in Western Australia (Perth hills, Manjimup/Donny- (2004) found that blue attracted more hoverflies (Allograpta obli- brook), New South Wales (Central West Coast, Sydney Basin), qua (Say)) than yellow or white traps in their trials in broccoli. The Queensland (Granite Belt), and Victoria (Goulburn Valley) (Hardy green lacewing Chrysoperla carnea (Stephens) showed a variable et al., 2005). ‘Pansy spots’ or ‘ghost spots’ were first reported in seasonal response to orange, red, black hues and clear traps in 2000 from apples (cv. Granny Smith, Red Delicious) in south- alfalfa (Blackmer et al., 2008). eastern Queensland, and in 2003/04 from apples (cv. Granny The development of thrips semiochemicals could further Ò Smith, Pink Lady) in the Perth hills. These spots result from enhance trap selectivity. Thriplineams developed by Keele Univer- oviposition sites over which scar tissue has developed (Cockfield sity, England (Hamilton and Kirk, 2003), and produced by Syngenta et al., 2007; Steiner, 2008), and are often surrounded by a larger Bioline Ltd (also marketed by Biobest as ThriPher), is a synthetic discolouration resembling a ‘pansy’ shape: red and green-skinned version of a sexual aggregation pheromone produced by male apples are most susceptible (Cockfield et al., 2007). Silvering of F. occidentalis. Lurem-TR is a kairomone (interspecific) attractant nectarines was first reported in the 2002/03 season in Forbes, derived from host plants and related compounds (Teulon et al., Central Coast region of New South Wales, in 2002/03 in the Perth 2008b), developed by Plant Research International, the hills, Western Australia, and in the 2006/07 season in Swan Hill, Netherlands and Crop and Food Research New Zealand (van Tol Victoria (Mansfield and Lorimer, 2006). et al., 2007), and distributed by Koppert (2010). The semi- In efforts to control pests in orchards, growers are ochemicals differ in their attractancy to different thrips species. Ò encouraged to adopt Integrated Pest Management principles Thriplineams is species-specific, attracting male and female including the conservation of naturally occurring beneficial insects F. occidentalis, whilst Lurem-TR is interspecific, known to attract such as lacewings (Micromus tasmaniae (Walker), ), F. occidentalis, T. tabaci and Thrips major Uzel (Teulon et al., ladybirds (Coccinellidae) and hoverflies (Melangyna viridiceps 2008a,b). (Macquart), Syrphidae) which feed on and mites (Malipatil To minimise pesticide use and their effect on beneficial insects, et al., 2009). Growers can also release beneficials for the control growers should apply pesticides only when thrips are present. of pests such as phytoseiid mites (Phytoseiulus persimilis (Athias- Current recommendations for monitoring thrips are yellow sticky Henriot) and Typhlodromus occidentalis (Nesbitt)), for the control of traps and/or tapping buds or flowers (Hardy et al., 2005). The two-spotted mite (Tetranychus urticae (Koch)). present study compares the effectiveness of tapping versus trap- Effective thrips control, however, relies on pesticide applications ping at triggering the pesticide application action threshold for due to a lack of alternative control measures for field crops in thrips in deciduous fruit trees; and aims to identify the optimal trap Australia (Broughton and Herron, 2009). To successfully manage colour and semiochemical combination for monitoring thrips, thrips, correct identification of the damaging species is critical due particularly F. occidentalis, whilst being the least detrimental to to the resistance of F. occidentalis to a range of insecticides from beneficial insects. different chemical classes including synthetic pyrethroids, organ- ophosphates, and carbamates (Herron and Gullick, 2001), and newer chemistries such as fipronil and spinosad (Herron and James, 2. Materials and methods 2005). Insecticides applied at flowering to control T. imaginis such as tau-fluvalinate (synthetic pyrethroid), dimethoate (organo- 2.1. Field sites phosphate), or methomyl (carbamate) are not as effective against F. occidentalis. Spinosad effectively controls F. occidentalis (if pop- Trials were conducted on commercial farms in the Perth Hills, ulations are not compromised by resistance), is regarded to be southwestern Australia, which had previously sustained organic, is relatively safe to use with many beneficial insects, but is F. occidentalis damage (Table 1). This region has a Mediterranean e not effective against T. imaginis. climate with hot, dry summers (December February) and cool, wet e In plum orchards in South Africa, Allsopp (2010) found that blue winters (June August). Mean monthly daily air temperatures range e traps caught more F. occidentalis and F. schultzei than yellow traps. from 16.2 to 18.2 C (min) to 22.3 36.0 C (max) in summer, and e e Matteson and Terry (1992) have shown that F. occidentalis are 8.5 13.6 C (min) to 19.3 25.7 C (max) in winter; most rainfall is e > attracted to the brightness of the blue wavelength in cotton, and received in June August ( 100 mm/month) (BOM, 2011). F. occi- blue traps have been reported to catch more F. occidentalis in dentalis are present all year, but are most abundant from October to glasshouse (Brødsgaard, 1989; Gillespie and Vernon, 1990) and field April (Broughton unpubl. data). No control of F. occidentalis was crops (broccoli, Chen et al., 2004; lettuce and onion, Natwick et al., carried out during trap trials, though control was carried out fl 2007). White (Yudin et al., 1987) and yellow (Cho et al., 1995) traps against other pests such as Mediterranean fruit y(Ceratitis cap- have also been reported to catch F. occidentalis in open lettuce and itata (Wiedemann)) with organophosphate insecticides. tomato crops, respectively. Low ultra-violet reflecting white, blue and yellow water traps have been shown to catch more T. imaginis than green, red, black and high ultra-violet reflecting white (Kirk, Table 1 1984). Trap sites.

The few studies on the effect of trap colour on capture of Orchard Cultivars Location Latitude and longitude beneficial insects suggest a variable response. Clare et al. (2000) A Red Roy, August Red Roleystone S32 010390, E116060388 and Wallis and Shaw (2008) evaluated the effect of red, green, (nectarines) white, yellow and blue traps on capture of beneficial species in New B Rose Diamond/Spring Pickering S32 010725, E11606.963 Zealand apple orchards. White attracted more honey (Apis mellifera Bright (nectarines) Brook L.) and native bees (Lasioglossum, Hylaeus spp.), blue attracted more C Arctic Star/Spring Karragullen S32 06.101, E116 07.171 Bright (nectarines) bumble bees (Bombus spp.) (Clare et al., 2000), whilst yellow traps D Pink Lady (apple), Karragullen S32 06.673, E116 07.541 attracted more parasitic wasps (Wallis and Shaw, 2008). Yellow Rose Diamond traps also attracted more seven-spotted ladybird, Coccinella sep- (nectarine) tempunctata (L.), in alfalfa (Maredia et al., 1992), and aphidopha- E Sundowner (apple), Karragullen S32 05.435, E116 07.293 gous hoverflies (Laubertie et al., 2006) including Melangyna spp. in Arctic Star (nectarine) 158 S. Broughton, J. Harrison / Crop Protection 42 (2012) 156e163

2.2. Experiment 1 e trapping vs. tapping and standard yellow and D3 at fruit ripening. The experimental design was the same as sticky traps vs. ‘Seabright’ blue traps for experiment 1, except that yellow wet sticky traps were baited Ò Ò with Thriplineams or unbaited (control). Thriplineams consisted of Two monitoring methods (trapping or tapping buds/flowers) a cone-shaped rubber septa (18 mm long, 4 mm base to 9 mm diam. were compared by counting the number of times that either top of septa) impregnated with pheromone. The septum was method (traps, direct sampling) triggered the action threshold (1 attached to one side of the trap approximately 3 cm from the top. individual of an economic thrips species; Hardy et al., 2005). Syngenta (2011) recommends traps with lures to be placed 10 m Methods were compared for 13 weeks from 6 September to 29 apart under glasshouse conditions. Based on field experiments, November 2007 (spring) in nectarines at four farms in the Perth Teulon et al. (2008a) suggest that odour lures can influence trap Hills (orchards A1, B1, B2, C1, C2 and E1, Table 1). Each farm con- capture of thrips on traps without odour lures 10 m away. Conse- sisted of orchards with rows of trees of a single cultivar and age, quently, trap pairs were placed 15 m apart, 1.5e2.0 m from the ranging in size from 0.2 to 1.5 ha (Table 1). ground. Traps were removed and replaced every 7 days. Trap colour was compared with a ‘pseudo’ randomised block design of blocks of trees of different cultivars spatially separated 2.4.2. Experiment 4 e Lurem-TR with blue sticky traps within and between orchards. Each orchard was divided into two This experiment was carried out in orchards A1, B2, D1 and D3 areas of equal size (¼block), with a pair of trees (¼plot) randomly from fruit development (4 cm) to harvest (24 Novembere8 selected from each block. Paired trees were 25 m apart; with 5e8 December 2009, spring-summer). The experimental layout was trees between pairs depending on tree spacing, which varied the same as experiment 3, except that Lurem-TR and blue wet from farm to farm. One of the two treatments (blue or yellow trap) sticky traps (Seabright Enterprises) were used. Lurem-TR consisted was randomly allocated to each plot at random. At flowering, a wet of a clear plastic package with a plastic hook. The pheromone sticky yellow (Bugs for Bugs, Munduberra, Queensland) or blue trap was impregnated in a 2.6 cm wide 4.4 cm long pad (total (Seabright Blue Thrips/Leaf miner traps, Seabright Enterprises, area ¼ 11.44 cm), covered by a perforated plastic membrane. The Emeryville, CA) were hung in the host canopy 15 m apart and entire back of the lure was further covered with a foil cover. The 1.5e2.0 m from the ground, and at least 25 m apart. Traps were lure was secured to the trap and the foil cover removed to allow 10.2 cm wide 12.5 cm high (total area 225 cm2) and pre-coated on the pheromone to disperse. Pheromones and traps were removed both sides with sticky adhesive. Traps were removed and replaced and replaced each week. every 7 days, at which time trap colour was randomly re-assigned over a period of 14 weeks. To account for potential differences in 2.5. Insect identification thrips distribution, ‘plot’ positions were also randomly assigned. Over the same period in conjunction with the trapping, ten trees Adult thrips caught on sticky traps and collected from tapping were randomly selected for tapping from the same orchards samples were identified to species in the laboratory under a dis- (Table 1). Five branches were randomly selected from each tree and secting binocular microscope using the criteria of Moritz et al. fl the buds, owers and leaves were tapped sharply over a yellow (2001). Beneficials insects were identified to species based on plastic plate (40 cm diameter). Any thrips present (adults and descriptions provided in Malipatil et al. (2009), and confirmed with fi larvae) were collected using a ne paintbrush into labelled vials the DAFWA Entomology Curator, Mr. A. Szito. containing 70% alcohol for processing in the laboratory. 2.6. Statistical analysis 2.3. Experiment 2 e comparative trial: MAFF (Ministry of Agriculture and Forestry) trap bases To determine any correlation between the number of thrips caught on traps (F. occidentalis, T. imaginis) and those obtained from The effect of six trap colours (white, blue, green, yellow, black tapping samples, the mean number of thrips/trap was regressed and red) and a control (clear) on capture of thrips and beneficial against the mean number of thrips/tree/week for each sampling insects was evaluated on two orchards (A2, D3; Table 1). A rando- date. mised block design was used, with blocks comprised of Experiments 1, 3 and 4 were analysed by ANOVA. Orchard, plot orchard cultivar week. Trapping was carried out over an 8 week and cultivar were included as blocking factors, and trap colour (or period from 23 October to 6 November 2008 (spring, flowering) on lure) as the treatment factor. Least significant differences (LSD) are trellised nectarines. Orchards were divided into four contiguous presented in figures at P ¼ 0.05. A skeleton of the ANOVA table for areas or ‘blocks’, with six treatments (trap colours) including a clear experiment 1 appears below (Table 2), and similar ANOVAs were control trap per block. Each block consisted of three rows of trees used to analyse data in experiments 3 and 4. spaced 1.6 m apart and 11.2 m long in orchard D3, and three rows of Experiment 2 was also analysed by ANOVA with orchard, block trees spaced 2 m apart and 14 m long in orchard B3. Traps were and plot included as blocking factors, and trap colour as a treatment suspended from the middle row of each block, 1.5 m from the factor. The total number of thrips or beneficials caught/trap was ground and 1.2 m (orchard B3) to 2 m apart (orchard D3). CorfluteÔ transformed (square root x þ 0.5) prior to all analyses to stabilize coloured traps, 18 cm wide 19 cm high (total area 342 cm2), and Ò variances. Residual plots of the transformed data were examined to a clear trap (Mylar sheet, 18 cm 19 cm) were sourced from the Ministry of Agriculture and Forestry (MAF), New Zealand. One side of each trap was coated with a layer of wet sticky adhesive Table 2 Ò (Tanglefoot Tangle-TrapÔ Insect Trap Coating, The Tanglefoot Skeleton ANOVA table for experiment 1.

Company, Grand Rapids, Michigan, USA). Source of variation Degrees of freedom Orchard 4 2.4. Thrips semiochemicals Orchard.cultivar.plot 5 Treatment (¼trap colour) 1 Ò Residual 11 2.4.1. Experiment 3 e Thriplineams with yellow sticky traps This experiment was conducted over an 8 week period in summer Orchard.cultivar.plot.week [SAMPLING] 276 Total 299 (19 Februarye12 March 2009) in nectarine orchards A1, B1, and D1 S. Broughton, J. Harrison / Crop Protection 42 (2012) 156e163 159 ensure that data were normal. GenStat for Windows 14th edition 15 Frankliniella occidentalis (VSN International Ltd, Hempstead, UK) was used for all statistical analyses. 10 3. Results and discussion

3.1. Tapping vs. trapping 5

For trapping to be an effective monitoring tool, the number of 0.5)) + (x (sqrt thrips caught on traps should be correlated with the number of 30 4 thrips on the crop. In this study, there was poor correlation thrips/treatment No. Mean 0 2 blue yellow between trap catches and tapping samples (R ranging from 0.00 to 15 0.05; Table 3). Tapping was less likely to trigger an action threshold Thrips imaginis than trapping, and yielded less than 1% of the number of thrips caught on sticky traps (Table 3). In a study of nectarines in British Columbia, Canada, Pearsall and Myers (2000) found that pop- 10 ulations of adult and larval F. occidentalis were highly aggregated in flower buds, but were randomly distributed during other phaeno- logical stages. They found that beating boards and trapping were 5 not as effective as flower dissections at detecting F. occidentalis, and (x+0.5)) (sqrt adults and larvae were present in buds before they were detected in traps. However, dissection of 2450 nectarine buds and flowers 43 51 collected in the 2006/07 and 2007/08 seasons (S. Broughton thrips/treatment No. Mean 0 blue yellow unpubl. data) yielded T. imaginis and T. tabaci, but no F. occidentalis. 15 fl These data suggest that during owering in nectarines and plums, Thrips tabaci F. occidentalis are unlikely to be a problem in Australia, as has been suggested by Hardy et al. (2005). Later in the season (OctobereNovember), however, peaks in the number of thrips 10 caught on traps were followed by detection of thrips in tapping samples 1e2 weeks later. This corresponds with fruit development- maturity in nectarines and plums, and flowering in apples, and is 5 the period when growers have previously reported F. occidentalis (x+0.5)) (sqrt damage. These data suggest that F. occidentalis aggregate on deciduous fruit trees later in the season, and trapping would be 17 15 more appropriately used as an early warning tool at this time. thrips/treatment No. Mean 0 blue yellow Growers should keep in mind, however, that there is a lag time between trap catches and thrips moving onto flowers and fruit. Fig. 1. Comparison of the number of adult thrips caught (F. occidentalis, T. imaginis and T. tabaci) on blue and yellow wet sticky traps. The error bar is 5% LSD/2. Non- overlapping bars indicate significant differences. Numbers within bars are the back- 3.2. Response of thrips to coloured traps transformed means.

The results from experiment 1 (mean number of adult F. occidentalis, T. imaginis or T. tabaci caught per treatment) are caught on blue compared to yellow traps (Fig. 1). However, there shown in Fig. 1. A total of 23,161 adult thrips were counted and were no differences in the capture of either T. imaginis (F ¼ 0.15, identified in experiment 1, with T. imaginis the most abundant df ¼ 1,9, P > 0.05) or T. tabaci (F ¼ 3.33, df ¼ 1,9, P > 0.05) on species, followed by F. occidentalis (8.9%) and T. tabaci (4.6%) (Fig. 1). ‘Seabright’ blue or yellow traps (Fig. 1). Trap colour had a significant effect on capture of F. occidentalis In experiment 2, T. imaginis (92.74%), T. tabaci (5.55%) and (F ¼ 29.73, df ¼ 1,9, P < 0.001), with two times more F. occidentalis F. occidentalis (0.30%) were the most abundant species (n ¼ 10,323 adult thrips). Too few F. occidentalis were caught to evaluate a preference for different trap colours, and all three species were Table 3 Comparison of the number of times the action threshold (1 thrips/sample; Hardy pooled for statistical analysis. Approximately three times more et al. 2005) is triggered when tapping (buds, flowers, foliage) or sticky traps. thrips were caught on blue, yellow and white bases, than clear, red, green or black bases (F ¼ 49.03, df ¼ 6, 45, P < 0.0001; Fig. 2). Traps Orchard Tapping Yellow Blue Correlation between No. thrips caught on with green bases caught three times fewer thrips than blue traps, traps and tapping (r2), with a mean of 24 thrips/trap/week, while red and black bases and F, df and P values clear traps (control) caught less than 7 thrips/trap/week (Fig. 2). A, Red Roy 3 13 13 r2 ¼ 0.03, F ¼ 12.18, Separate analysis of trap colour for T. imaginis showed a preference df ¼ 1,7, P ¼ 0.01 for blue, yellow and white bases, over red, green or black bases or 2 B, Rose Diamond 4 13 13 r ¼ 0.0009, F ¼ 0.11 ¼ ¼ < ¼ ¼ clear traps (F 77.41, df 6, 42, P 0.001, Fig. 2). Kirk (1984) also df 1,11, P ns fl C, Spring Bright 6 13 9 r2 ¼ 0.05, F ¼ 0.006, found that blue yellow, and white low ultra-violet re ecting water df ¼ 1,11, P ¼ ns traps caught more T. imaginis than green, red, black or high ultra- D, Rose Diamond 6 13 13 r2 ¼ 0.03, F ¼ 0.35, violet reflecting white. Whilst Natwick et al. (2007) found that df ¼ 1,11, P ¼ ns more T. tabaci were caught on blue traps than yellow traps in a trial E, Arctic Star 4 13 13 r2 ¼ 0.07, F ¼ 0.87, in lettuce and onion crops, there were no differences in capture of df ¼ 1,11, P ¼ ns T. tabaci on blue or yellow traps in experiments 1 or 2. 160 S. Broughton, J. Harrison / Crop Protection 42 (2012) 156e163

10 economically important species 10 Frankliniella occidentalis

8 8

6 6 4

4 2

No. thrips/treatment (sqrt x + 0.5) x (sqrt thrips/treatment No. 14 44 2 0 no lure Thripline 579724 6 76 71 Mean No. adults/trapMean (sqrt + x 0.5) 0 10 Thrips imaginis black blue clear green red white yellow 8

10 Thrips imaginis 6

4 8

2 6 No. thrips/treatment (sqrt x + 0.5) 43 0 no lure Thripline 4 Fig. 3. Comparison of the number of adult F. occidentalis caught on baited (Thripline) vs. unbaited traps. The error bar is 5% LSD/2. Non-overlapping bars indicate significant differences. Numbers within bars are the back-transformed means. 2

Mean No. thrips /trap (sqrt x + 0.5) x (sqrt /trap thrips No. Mean 574723 6 72 68 fruits mature in nectarines in particular, the odours emitted from 0 the developing fruit may account for poor performance against black blue clear green red white yellow T. tabaci. In addition to improving trap selectivity, semiochemicals could Fig. 2. Comparison of the number of adult thrips (all species combined) and T. imaginis be used in mass trapping to reduce thrips populations. Of the caught on different coloured traps. The error bar is 5% LSD/2. Non-overlapping bars fi indicate significant differences. Numbers within bars are the back-transformed means. factors identi ed by El-Sayed et al. (2006) that contribute to the success or failure of mass trapping programs, isolation and low population density of the target pest are key factors contributing to 3.3. Effect of semiochemicals on thrips catches success. F. occidentalis do not appear to colonise native Australian vegetation (Schellhorn et al., 2010), and most sources of The addition of semiochemicals to traps increased capture of F. occidentalis that occur on orchards are likely to be on weeds early F. occidentalis in experiments 3 and 4 (Fig. 3). Thripline (sexual in the season. Based on trapping, overwintering of F. occidentalis aggregation pheromone) increased the capture of F. occidentalis by occurs in the orchard in low numbers in weeds (Broughton unpub. three times compared to unbaited traps (F ¼ 31.78, df ¼ 1, 31, data). Semiochemicals may be useful in reducing this over- P < 0.001) (Fig. 3). Thripline had no effect on capture of either T. wintering population of F. occidentalis, though further research imaginis or T. tabaci (P > 0.05), confirming that it is a species- would need to determine optimum trap density, lure competi- specific lure. tiveness, and lure longevity (El-Sayed et al., 2006). Lurem-TR (kairomone) significantly increased the capture of F. occidentalis, also by three times compared to unbaited traps (F ¼ 23.74, df ¼ 1,87, P < 0.001; Fig. 4). Lurem-TR also significantly 3.4. Response of beneficial insects to visual and odour cues increased the capture of T. imaginis by 1.4 times (F ¼ 53.81, df ¼ 1,87, P < 0.001), but had no effect on T. tabaci (F ¼ 2.28, df ¼ 1,87, P ¼ ns, The mean number of beneficial insects caught per trap per week Fig. 3). The increased capture of F. occidentalis and T. imaginis on on blue and yellow sticky traps (Experiment 1) is shown in Fig. 5.A traps baited with Lurem-TR was not unexpected, as glasshouse and total of 3969 beneficial insects were caught, with hoverflies field trials in Europe and New Zealand have shown that Lurem-TR (M. viridiceps, 74.3% total catch) and brown lacewings shows activity against other thrips species (Teulon et al., 2008a,b; (M. tasmaniae, 23.0% total catch) the most abundant species. Nielsen et al., 2010). Davidson et al. (2009) and Nielsen et al. (2010) Ladybirds (Hippodamia variegata (Goeze), Coccinella transversalis suggest that extrinsic (e.g. temperature, humidity) and intrinsic Fabricius) and green lacewings (Mallada spp.) comprised 2% of the factors (e.g. age, nutritional status) influence thrips responses to total. In experiment 1, 1.4 times more beneficials caught on blue semiochemicals. Davidson et al. (2009) found that trap catches of compared to yellow traps (F ¼ 19.6, df ¼ 1,9, P ¼ 0.002). Results T. tabaci were much higher in grass fields (84 more) (a non-host) from experiment 2 comparing trap catches on white, blue, green, on traps baited with ethyl isonicotinate, methyl isonicotinate, and yellow, black, red, and clear traps are shown in Fig. 6. A total of 1452 ethyl nicotinate, than an onion crop (18) (host plant) in field trials, insects were counted and identified, with brown lacewings suggesting that host plant odours may mask the lure odour. As (M. tasmaniae, 72.5%) the most abundant species, followed by S. Broughton, J. Harrison / Crop Protection 42 (2012) 156e163 161

20 5 all beneficial insects Frankliniella occidentalis 4 15 3 10 2

5 (x+0.5)) (sqrt 1 16 11

5 17 Mean No. adults/treatment 0 Mean no. thrips/treatment (sqrt x + 0.5) 0 blue yellow no lure Lurem 5 20 Thrips imaginis Micromus tasmaniae 4 15 3

10 2

(sqrt (x+0.5)) (sqrt 1 5 45

Mean No. adults/treatment 0 121 245

Mean No. thrips/treatment (sqrt + 0.5) blue yellow 0 no lure Lurem 5 Melangyna viridisceps 20 Thrips tabaci 4

15 3

2 10 (sqrt (x+0.5)) (sqrt 1

5 13 7 Mean No. adults/treatment No. Mean 0 blue yellow 3 4 0 Fig. 5. Comparison of catches of all beneficial insects (ladybirds, lacewings and hov- Mean no. thrips/treatment(sqrt + 0.5) no lure Lurem erflies) and M. tasmaniae, M. viridiceps on blue and yellow sticky traps. The error bar is 5% LSD/2. Non-overlapping bars indicate significant differences. Numbers within bars Fig. 4. Comparison of the number of adult F. occidentalis, T. imaginis and T. tabaci are the back-transformed means. caught on baited (Lurem-TR) vs. unbaited traps. The error bar is 5% LSD/2. Non- overlapping bars indicate significant differences. Numbers within bars are the back- transformed means. more attractive to hoverflies (A. obliqua) than yellow or white in their trials in broccoli. Brown lacewings (M. tasmaniae) showed hoverflies (M. viridiceps; 24.3%) and ladybirds (H. variegata, more variability in their response to coloured traps than hoverflies. C. transversalis, 3.2%). Significantly more beneficials were caught on More M. tasmaniae (1.25 times more) were caught on yellow traps blue traps than other trap colours (Fig. 6; species pooled; F ¼ 9.54, in experiment 1 (F ¼ 14.5, df ¼ 1,9, P ¼ 0.004). In experiment 2, 1.3 df ¼ 6,42, P < 0.001), with a mean of 10 beneficials/trap/week times more brown lacewings were caught on blue (mean 5/trap), caught on blue traps, compared to less than 6 beneficials/trap/week black (mean 6/trap), and red traps (mean 6/trap), than clear traps on yellow, white, red, blue, and green traps. Clear traps were the (control, mean 2/trap; Fig. 6). safest to use with beneficials, with a mean of 3 beneficials caught The addition of semiochemicals (experiments 3 and 4) appeared trap/week, but were not practical for monitoring thrips. to have no effect on the overall catch of beneficial insects (data not Approximately two times more hoverflies were caught on the shown). No beneficial insects were caught during the experiment Ò ‘Seabright’ blue than the standard yellow trap (F ¼ 42.4, df ¼ 1,9, with Thriplineams, and there were no differences in the catch of P < 0.001). In experiment 2, six times more M. viridiceps were beneficials on traps baited with Lurem-TR compared to the control caught on blue and white traps compared to the other trap colours (F ¼ 0.14, df ¼ 1,87, P ¼ 0.71). However, separate analyses by species including yellow. This result contrasts with Bowie et al. (1999), who showed that 1.3 more brown lacewings were caught on traps baited found that yellow pan traps caught more M. viridiceps in their trials with Lurem-TR than unbaited traps (F ¼ 12.07, df ¼ 1,86; P ¼ 0.001) of six pan trap colours in wheat in New South Wales, Australia. Lurem-TR 2.2 (trap/week, unbaited 1.7/trap/week), but had no Yellow pan traps (wavelengths of 520e700 nm) are also used in effect on the capture of hoverflies (F ¼ 3.36, df ¼ 1,87, P ¼ 0.07). New Zealand to monitor populations of insects with potential Since Lurem-TR is a food attractant derived from host plants and value for biological control, including hoverflies (Bowie et al., related compounds (Teulon et al., 2008b), the results suggests that 2003). However, Chen et al. (2004) found that blue traps were M. signata may be responding to similar cues. 162 S. Broughton, J. Harrison / Crop Protection 42 (2012) 156e163

4 attracted 1.6 times more beneficial insects (brown lacewings, hov- all beneficial insects erflies and ladybirds). The addition of semiochemicals increased capture of F. occidentalis by three times compared to unbaited traps. Ò Thriplineams, attracted F. occidentalis, but had no effect on the 3 capture of T. imaginis or T. tabaci. Lurem-TR attracted more F. occidentalis, and increased the capture of T. imaginis by 1.3 times. Whilst semiochemicals did not affect the overall capture of bene- 2 ficial insects, yellow traps baited with Lurem-TR caught 1.3 times more brown lacewings than unbaited traps. Based on these results, growers wanting to selectively monitor for F. occidentalis should use blue sticky traps, but are also likely to 1 also trap more beneficial insects. Selectivity can be improved by Ò adding Thriplineams to the trap. Manufacturer’s recommendations 6103 5665 suggest that the semiochemicals last for 4e6 weeks, which would Mean No. adults/trap (sqrt x + 0.5) + x (sqrt adults/trap No. Mean 0 make the use of semiochemicals an affordable option if lures are black blue clear green red white yellow reused when traps are replaced each week.

3 Melangyna viridiceps Acknowledgements

We would like to thank David Cousins for his help in the field and in the laboratory. Thanks also to Grant Herron and David 2 Teulon for reading earlier drafts of the paper and anonymous reviewers for their critical comments. Mario D’Antuono and Touhid Rahman provided helpful advice on statistical analyses. Ric Owen, Ron Fry, Tony Vincenti, John Vetta and Gary Scolaro generously allowed access to their properties for research. Horticulture 1 Australia Ltd and DAFWA helped to fund this research through project MT 06001.

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