Action: Use chemicals to attract natural enemies
Parasitism and predation (by natural enemies): One review and two of five studies from Asia, Europe and North America found that attractive chemicals increased parasitism. Two studies, including one randomised, replicated, controlled trial, found greater parasitism for some but not all chemicals, crops, sites or years and one study found no effect. One study showed that parasites found pests more rapidly. One study found lower egg predation by natural predators.
Natural enemies: Five of 13 studies from Africa, Asia, Australasia, Europe and North America found more natural enemies while eight (including seven randomised, replicated, controlled trials) found positive effects varied between enemy groups, sites or study dates. Four of 13 studies (including a meta-analysis) found more natural enemies with some but not all test chemicals. Two of four studies (including a review) found higher chemical doses attracted more enemies, but one study found lower doses were more effective and one found no effect.
Pests: Three of nine studies (seven randomised, replicated, controlled) from Asia, Australasia, Europe and North America found fewer pests, although the effect occurred only in the egg stage in one study. Two studies found more pests and four found no effect.
Crop damage: One study found reduced damage with some chemicals but not others, and one study found no effect.
Yield: One study found higher wheat yields.
Crops studied were apple, banana, bean, broccoli, Chinese cabbage, cotton, cowpea, cranberry, grape, grapefruit, hop, maize, oilseed, orange, tomato, turnip and wheat.
This involves using chemicals to lure natural enemies into a crop. Communication chemicals of insects and plants (known as pheromones and volatiles, respectively) can be manufactured and deployed to manipulate invertebrates. Examples include the volatiles produced when plants are attacked by pests (e.g. methyl salicylate) and the alarm and sex pheromones of pests or natural enemies, as well as organic extracts from crop or plant leaves. Chemicals are sprayed onto crops or deployed in dispensers placed at regular intervals in the crop. Many studies have tested the efficacy of chemicals by applying them as baits in insect traps such as delta traps (plastic structures hung from branches or posts containing a sheet of sticky paper). Ground-living invertebrates can be sampled by suction sampling, using a vacuum to suck-up and collect specimens for a given time or area of ground.
Supporting evidence from individual studies
A controlled, paired study in Egypt (McVeigh et al. 1983) found three times more insect predators in cotton Gossypium sp. fields treated with pink bollworm Pectinophora gossypiella mating-disruption chemicals (sex pheromones) than in controls treated with insecticide. Average daily moth (Lepidoptera) catches were lower and seed cotton yields were higher in fields treated with pheromones than in controls. Three sex pheromone formulations were tested (microcapsules in solution, laminated plastic chips and hollow fibres) but average moth catches and yield were unaffected by these treatments. Pheromone treatments were tested in three 50 ha blocks of cotton, each paired with a 50 ha insecticide-treated control. Natural enemies were monitored by D-vac sampling. Moths were monitored in pheromone-baited traps and by counting infested flowers and cotton bolls. This conference paper did not determine whether natural enemies were attracted to the pheromones or simply benefited from the absence of insecticides.
A replicated, controlled field study (Nordlund et al. 1985) found greater corn earworm Helicoverpa zea parasitism in plots of corn Zea mays treated with tomato Solanum lycopersicum extract (38% eggs parasitised) than in control plots of corn without tomato extract (29%). Eggs were parasitised by the wasp Trichogramma pretiosum. Parasitism was similar in plots of tomato treated with corn extract (53% eggs parasitised) and controls of tomato without corn extract (54%). A greenhouse experiment found the wasp also parasitised more corn earworm eggs in pots of cowpea Vigna unguiculata treated with tomato extract (52-74% eggs parasitised) than in pots treated with corn extract (19-26%) or untreated controls (18-26%). A lab study found similar results by monitoring parasitism in petri dishes containing the extracts. Plant extracts were obtained by grinding fresh leaves. In the field study extracts were sprayed (at 2 g/plot in 10 ml of hexane) on 1 row by 3 m plots. Controls were left unsprayed. Corn and tomato extract treatments were replicated 30 and 40 times, respectively. Corn earworm eggs were placed at 0.3 m intervals, 50 parasitoid wasps were released and eggs were collected after four hours. The greenhouse trial grew cowpea in 28.8-cm pots.
A replicated study in 1995 in Maryland, USA (Sant'Ana et al. 1997) found more predatory spined soldier bugs Podisus maculiventris in six green bean Phaseolus vulgaris rows positioned close to pheromone chemical dispensers (averaging 4 immature spined soldier bugs) than in six bean rows further away (1 immature). More spined solider bugs were recovered in the six closest (0.0-4.5% recovered) than the six farthest (0.0-1.4%) bean rows at four and seven days after their release, but numbers were similar one day after their release (0.0-1.3 vs. 0.0-1.6%). Numbers of the pest Mexican bean beetle Epilachna varivestis were similar in the six closest (11-20 larvae/row) and six farthest (5-39 larvae) rows from the pheromone dispensers. Immature spined solider bug were also attracted to the pheromone in a wind tunnel experiment. Three Soldier Bug Attractors (dispensers containing a pheromone produced by adult male spined solider bugs) were placed along one edge of a 13-row plot of green beans. Immature spined solider bugs were released into the middle row of the plot (averaging 261 individuals/plot) and monitored to assess their spread towards or away from the dispensers. Plots were 9.7 x 6.3 m and replicated seven times.
A randomised, replicated, controlled trial in 2004 in Washington State, USA (James et al. 2005) found more parasitic wasps from the genus Metaphycus in vineyard blocks baited with three chemical treatments (averaging 12-25 wasps/shake sample/week) than in unbaited controls (8 wasps). Chemicals attracted more wasps from the genus Anagrus than controls in 1-3 of the five months, but numbers were only greater in all three treatments in September (approximately 260-290 vs. 170-175 wasps/trap/week). A replicated, paired, controlled trial found hops Humulus lupulus with methyl salicylate had 3-5 times more predatory insects than unbaited hops. Hops with a low methyl salicylate deployment rate had more predators vs. hops with high deployment (106 vs. 46 predators/shake sample/week). Pest spider mites (Tetranychidae) briefly exceeded spraying thresholds in baited but not unbaited hops. Predators were scarce in vineyards but some groups, including hoverflies (Syrphidae), lacewings (Chrysopidae) and lady beetles Stethorus spp., were more numerous in baited than unbaited vineyards. The first study compared methyl salicylate, methyl jasmonate and (Z)-3-hexenyl acetate treatments with unbaited controls, replicated in three 8 x 30 m vineyard blocks. The second study tested methyl salicylate at rates of 0, 180 and 516-556 dispensers/ha in hops and vineyards.
A controlled study in 2003 in Guangzhou, China (Kong et al. 2005) found that more predatory mites Amblyseius newsami occurred in orange Citrus sinensis trees treated with essential oils of tropical whiteweed Ageratum conyzoides (0.41 mites/leaf) than on control trees (0.09 mites) after 24 hours. However, 48 hours after treatment, numbers of predatory mites had dropped to 0.13 mites/leaf. Fewer pest citrus red mites Panonychus citri were found on treated (0.05 mites/leaf) than control (0.18 mites) trees after 24 hours, but numbers increased to 0.19 mites/leaf on treated trees after 48 hours. A 5% emulsion of tropical whiteweed essential oil and a water control were applied to 18 and nine orange trees, respectively. All trees were more than 15 m apart. The authors found that a tropical whiteweed ground cover increased predatory mite numbers (see 'Grow non-crop plants that produce chemicals that attract natural enemies') and they suggest this may attract the predator for longer than using essential oils.
A randomised, replicated, controlled study in 2007 in Saint Méloir des Ondes, France (Ferry et al. 2009) found lower cabbage fly Delia radicum egg predation in broccoli Brassica oleracea plots with dimethyl disulphide lures (2.1 eggs predated/patch of eggs) than in controls without the chemical (2.6 eggs). More rove beetles (Aleochara bilineata and A. bipustulata) occurred in treated plots (119 and 107 individuals, respectively) than controls (21 and 69 individuals) and numbers were highest in pitfall traps closest to the chemical attractant. More ground beetles Bembidion spp. occurred in treated plots (539 individuals) than controls (462 individuals) but this effect varied with sampling date and there was no effect of distance from the chemical. Fewer cabbage fly eggs were found in treated plots than controls (4 vs. 11 eggs/plant), but larvae and pupae numbers were similar. Fly damage to broccoli was similar in the two treatments. Tubes of dimethyl disulphide diluted in paraffin were placed beside broccoli plants in treated plots. Controls used tubes of pure paraffin. Treatments were replicated four times in 14 x 15 m plots. Egg predation was measured by placing 16 patches of eggs (5 eggs/patch) into each plot for 48 hours and counting missing/chewed eggs.
A randomised, replicated, controlled study in 2007 in Canterbury, New Zealand (Orre et al. 2010) found higher numbers of the parasitoid wasp Diadegma semiclausum in turnip Brassica rapa plots with a methyl salicylate lure (averaging 1.6-7.2 wasps/trap) than in controls without the chemical (1.4-6.4 wasps). Other natural enemies, including brown lacewings Micromus tasmaniae and hoverflies (Syrphidae), were captured too infrequently to be analysed. More pest leaf miners Scaptomyza flava occurred in plots with the chemical attractant (2-17 leaf miners/trap) than controls (1-12 leaf miners). The parasitic wasp Anacharis zealandica, an enemy of beneficial brown lacewings, was also more abundant in plots with methyl salicylate (0.0-3.3 wasps/trap) than in controls (0.0-1.2 wasps). The authors suggest that attracting beneficial insects with chemicals can also attract potentially harmful insects. One sachet of synthetic methyl salicylate was hung above treated plots and was replenished twice during the study period (24 April to 12 June 2007). No chemical was used in controls. Treated and control plots were replicated 12 times in a 400 x 470 m field. Natural enemies, pests and parasites of natural enemies were monitored using yellow sticky traps.
A randomised, replicated, controlled experiment in 2006-2008 in Israel, Italy and Portugal (Franco et al. 2011) found greater citrus mealybug Planococcus citri parasitism in traps with lavandulyl senecioate lures (19-51 parasitoid wasps Anagyrus sp. emerged from citrus mealybugs/trap) than in control traps (0-20 wasps emerged) in seven of 10 trials. Parasitism was similar between traps in three trials (5-10 vs. 2-4 wasps emerged). Wasps took 1.6-3.5 fewer days to emerge from mealybugs collected from baited than from control traps, suggesting wasps had found baited traps more rapidly. More parasitoid wasps were found in baited (1-16 females/trap) than control (0-2 females) traps in five of nine trials, but very few wasps occurred in the four other trials (in both treatments). Parasitism levels and wasp numbers were similar between traps with lavandulyl isovalerate lures and control traps in four trials, and similar between traps with planococcyl acetate lures and controls in six out of seven trials. The dose of lavandulyl senecioate (ranging 25-1,000 µg) did not affect wasp numbers. The chemicals (all naturally released by mealybugs) were tested in citrus and banana plantations and vineyards at seven locations. Each treatment was replicated 5-14 times per site.
A controlled, replicated study in 1999 in Ibaraki Prefecture, Japan (Higaki & Adachi 2011) found greater parasitism of brown-winged green bugs Plautia stali in traps with an attractive chemical (6.0% individuals parasitized) than in control traps with light lures (2.7% parasitized). Parasitic flies Gymnosoma rotundatum were attracted to a chemical (methyl-2,4,6-decatrienoate) naturally produced by male brown-winged green bugs. In a separate experiment manipulating groups of bugs, the fly G. rotundatum parasitised 1-17% of bugs baited with the chemical compared to 0% for unbaited bugs. Monitoring from 2000 to 2005 found much fewer parasitic flies (approximately 25-95 adults captured at peak numbers) than brown-winged green bugs (260-9,710 adults) were attracted to traps with chemical lures. From April to November 1999, water-basin traps with 85 mg of methyl-2,4,6-decatrienoate were placed in Japanese paulownia Paulownia tomentosa trees and catches were compared with light traps (using 100 W mercury vapour lamps). In the second experiment (repeated six times) groups of 10 brown-winged green bugs were attached to frames with and without chemical lures and parasitism was monitored. Monitoring in 2000-2005 tested the lure in 2-5 water-basin traps/year from April to November.
A randomised, replicated, controlled study in 2008 in four apple Malus domestica orchards in Washington State, USA (Jones et al. 2011) found more green-eyed lacewings Chrysopa oculata (8-145 lacewings/trap) and green lacewings Chrysopa nigricornis (86-446 lacewings) in trees with iridodial-methyl salicylate lures than control trees without lures (0-3 and 0-7 lacewings, respectively). Benzaldehyde attracted higher numbers of the lacewing Chrysopa plorabunda in treated (6-64 lacewings/trap) compared to control trees (0-1 lacewings), but had little effect on green-eyed and green lacewing captures. Across all three species, there were mixed effects of iridodial alone, methyl salicylate alone, cis-3-hexen-1-ol and cis-3 hexenyl acetate. An additional experiment in two orchards found that squalene lures or mixed lures containing this chemical attracted more green lacewings (8-24 lacewings/trap day) than iridodial-methyl salicylate lures (2-4 lacewings). More green lacewings were caught with higher squalene doses. Six chemical lures (in 5-cm diameter plastic tubing) were placed in white plastic delta traps and compared with control traps containing distilled water. Each treatment was replicated four times in each orchard. Delta traps and lures were placed 1.5-3.0 m high in the canopy and lacewing captures were monitored 1-2 times/week.
A randomised, replicated, controlled study in 2008-2009 in cranberry Vaccinium macrocarpon bogs in New Jersey, USA (Rodriguez-Saona et al. 2011) found 4.5 times more hoverflies (Syrphidae), 1.8 times more lady beetles (Coccinellidae) and 7.6 times more green lacewings (Chrysopidae) in traps baited with methyl salicylate lures than in controls with no chemical. Baited traps had more hoverflies for seven of eight weeks but lady beetle and lacewing numbers were higher for only two of eight weeks. Flower bug (Anthocoridae), parasitoid fly (Tachinidae) and pest leafhopper (Cicadellidae) numbers were similar in the baited and control traps. In 2009, hoverflies were 84% more abundant in traps containing lures than in controls, but there was no effect for traps placed 2.5, 5 or 10 m away from lures. There was no effect of methyl salicylate on lady beetle numbers in 2009. A meta-analysis found 91 observations from 14 studies testing methyl salicylate lures on 34 natural enemy species (across nine crop types). Forty-one observations showed positive effects of lures and 50 showed no effect. The 2008 study applied single baited and control traps to 15 cranberry bogs, the 2009 study included 10 bogs (5 with lures, 5 with controls).
A randomised, replicated, controlled study in 2008-2009 in New South Wales, Australia (Simpson et al. 2011) found effects of attractant chemicals varied between crops and natural enemy groups. More predators occurred in broccoli Brassica oleracea treated with a mix of plant chemicals (2.5 predators/trap/day) than for water-treated controls (1.8 predators) one day after spraying. Attractants did not affect total predator numbers in sweetcorn Zea mays or grapevine Vitis vinifera and total parasitoid numbers were unaffected in all three crops. Two parasitoid wasp families (Ceraphronidae and Seclionidae) were attracted to one of four chemicals tested in broccoli and two families (Encyrtidae and Eulophidae) were attracted to one and all attractants respectively, tested in sweetcorn. However, some effects were short-lived or depended on the additional presence of attractive plants. Other natural enemy groups (including up to 11 parasitoid families and 10 predator groups) were not affected by chemical attractants. Butterflies and moths (Lepidoptera) and leafhoppers (Cicadellidae) were not attracted to plots with chemicals. Damage by moth larvae Helicoverpa sp. was lower in sweetcorn treated with methyl anthranilate attractant (1.5% sweetcorn damaged) than in controls (2.7%), but other chemicals had no effect. The study tested five plant chemicals (methyl anthranilate, methyl jasmonate, methyl salicylate, cis-3-hexenyl acetate and benzaldehyde) and two mixes of chemicals.
A randomised, replicated, controlled study in 2008-2009 in Shandong, China (Wang et al. 2011) found greater parasitism of English grain aphid Sitobion avenae in wheat Triticum aestivum plots containing methyl salicylate lures (averaging 23-26% aphids parasitised) than in controls without lures (18-19%). Aphid parasitism by wasps (Aphidiidae) increased to 27-29% when the chemical was released in wheat-oilseed rape Brassica napus intercrops. More predatory lady beetles (Coccinellidae) occurred in wheat monocrop and intercrop plots with lures (13-16 and 16-20 lady beetles/100 shoots, respectively) than in the monocrop control without lures (9-11 lady beetles). Fewer English grain aphids were found in plots with lures (approximately 455-520 and 345-380 aphids/100 shoots, in monoculture and intercropped plots respectively) than in the control (870-920 aphids). Wheat yields were also higher in plots with methyl salicylate lures (5.7-6.1 and 6.4-6.7 t/ha in monoculture and intercropped plots, respectively) compared to the control (5.3-5.4 t/ha). The study compared four treatments replicated three times: wheat monocrop (control), monocrop with methyl salicylate, wheat-oilseed rape intercrop, and intercrop with methyl salicylate. Methyl salicylate was released from one slow-release dispenser/plot at 120 mg/m²/week. Plots were 10 x 10 m and insects were monitored on 10 shoots at 10 sample sites/plot.
A randomised, replicated, controlled study in 2009-2010 in Shandong, China (Cui et al. 2012) found plots with E-β-farnesene lures had 9-41 parasitised aphids/20 Chinese cabbages Brassica rapa pekinensis compared to 5-19 parasitised aphids in controls. More parasitoid wasps (Aphidiidae) occurred in plots with the chemical attractant (11-14 wasps in traps) than controls (5-10 wasps). More lady beetles occurred on cabbages in treated versus control plots (14-16 vs. 6-8 lady beetles/20 cabbages), but numbers were similar in traps (2.4-3.0 vs. 0.7-2.7 lady beetles). Spider (Araneae) numbers were similar between treated plots (26-133 spiders/20 cabbages) and controls (60-104 spiders). Fewer aphids (Aphidoidea) occurred in plots with E-β-farnesene lures than controls (167 vs. 365 aphids/20 cabbages in 2009, 1,108 vs. 1,332 in 2010). A chemical releaser was attached to a yellow pan trap in the centre of each 10 x 10 m plot and filled with 100 µl of E-β-farnesene (an aphid alarm chemical) in paraffin oil every seven days. Controls used a pan trap with no chemical releaser. Treatments were replicated three times. Invertebrates were surveyed weekly in September-October on 20 cabbages and in pan traps.
A review (Kaplan 2012) of 35 studies found that 29 of 37 tested plant chemicals attracted and increased numbers of at least some natural enemy species or groups, although most chemicals also led to no response from other species or groups. One study (Titayavan & Altieri 1990) found that aphid (Aphidoidea) parasitism increased from 8.5% to 22.5% when broccoli Brassica oleracea was treated with allyl isothiocyanate. Williams et al. (2008) found two to three times more tarnished plant bug Lygus lineolaris egg parasitism when the chemicals (Z)-3-hexenyl acetate and α-farnesene were applied to cotton Gossypium hirsutum. One study (James & Price 2004) found densities of predatory insects were four times greater in hops Humulus lupulus baited with methyl salicylate compared to unbaited controls. Average numbers of minute pirate bugs Orius tristicolor and spider mite destroyers Stethorus punctum picipes were seven and 57 times greater (respectively) in baited than unbaited plots across the season. Another study in cotton (Flint et al. 1981) found that predatory beetle Collops vittatus numbers increased (from 0 to 2.7, 3.3 and 7.6 trap catches) as doses of synthetic caryophyllene oxide increased (0.0, 0.1, 1.0 and 10.0 g, respectively). James (2006) also found a dosage effect, with twice as many green lacewings Chrysopa oculata on traps baited with 99% methyl salicylate compared with 1% and 10% dilutions.
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