Introduction
Plants attacked by herbivorous insects may release volatile signals, which cause neighbouring intact plants to become ‘repellent’ to incoming herbivores and ‘attractive’ to predators and parasitoids (Pickett et al., Reference Pickett, Rasmussen, Woodcock, Matthes and Napier2003). (Z)-Jasmone, which is associated with the stress-induced jasmonic acid or octadecanoid pathway, is one such compound (Loughrin et al., Reference Loughrin, Manukian, Heath and Tumlinson1995; Paré & Tumlinson, Reference Paré and Tumlinson1997). (Z)-Jasmone was identified initially from the volatile profile of the black currant, Ribes nigrum L., the primary host of the currant–lettuce aphid, Nasonovia ribis-nigri (Mosley) (Hemiptera: Aphididae). Behavioural assays, using a four-arm olfactometer, showed (Z)-jasmone to be repellent to spring and summer aphid morphs, which fly to secondary hosts including lettuce, Lactuca sativa L. (Birkett et al., Reference Birkett, Campbell, Chamberlain, Guerrieri, Hick, Martin, Matthes, Napier, Pickett, Poppy, Pow, Pye, Smart, Wadhams, Wadhams and Woodcock2000). However, the effects of (Z)-jasmone were not restricted to N. ribis-nigri. In the same study, yellow water traps fitted with sachets releasing this compound caught significantly fewer spring migrants of the damson–hop aphid, Phorodon humuli (Schrank) (Hemiptera: Aphididae), than control traps. Similarly, plots of winter wheat, Triticum aestivum L., sprayed with (Z)-jasmone were infested by significantly fewer cereal aphids, including Metopolophium dirhodum (Walker), Sitobion avenae (Fabricius) and Rhopalosiphum padi (Linnaeus) (all Hemiptera: Aphididae) (Birkett et al., Reference Birkett, Campbell, Chamberlain, Guerrieri, Hick, Martin, Matthes, Napier, Pickett, Poppy, Pow, Pye, Smart, Wadhams, Wadhams and Woodcock2000; Bruce et al., Reference Bruce, Martin, Pickett, Pye, Smart and Wadhams2003), than unsprayed plants. By contrast with the responses of these aphid species, in olfactometer and wind tunnel studies, (Z)-jasmone evoked positive behavioural responses in an aphidophage, the seven-spot ladybird, Coccinella septempunctata Linnaeus (Coleoptera: Coccinellidae), and in an aphid parasitoid, Aphidius ervi Haliday (Hymenoptera: Braconidae) (Birkett et al., Reference Birkett, Campbell, Chamberlain, Guerrieri, Hick, Martin, Matthes, Napier, Pickett, Poppy, Pow, Pye, Smart, Wadhams, Wadhams and Woodcock2000).
Intact bean plants (Vicia faba L.) treated with (Z)-jasmone, at an initial concentration of 0.1 ppm in a closed glass vessel, were found to produce increased levels of (E,E)-α-farnesene, β-caryophyllene, (E)-4,8-dimethyl-1,3,7-nonatriene and (E)-β-ocimene (Birkett et al., Reference Birkett, Campbell, Chamberlain, Guerrieri, Hick, Martin, Matthes, Napier, Pickett, Poppy, Pow, Pye, Smart, Wadhams, Wadhams and Woodcock2000), compounds which have previously been shown to be released by plants attacked by herbivorous insects (Turlings et al., Reference Turlings, Loughrin, McCall, Röse, Lewis and Tumlinson1995). This result suggests that (Z)-jasmone may act as a phytopheromone, influencing the release of volatiles from neighbouring intact plants (Birkett et al., Reference Birkett, Campbell, Chamberlain, Guerrieri, Hick, Martin, Matthes, Napier, Pickett, Poppy, Pow, Pye, Smart, Wadhams, Wadhams and Woodcock2000; Chamberlain et al., Reference Chamberlain, Guerrieri, Pennacchio, Pettersson, Pickett, Poppy, Powell, Wadhams and Woodcock2001). Interestingly, after about 24 h, no remaining (Z)-jasmone could be detected in the glass vessel; however, structurally similar and biosynthetically related contaminants of the commercial (Z)-jasmone used were still present. It has, therefore, been suggested that the (Z)-jasmone is taken up selectively by the bean plant (Chamberlain et al., Reference Chamberlain, Guerrieri, Pennacchio, Pettersson, Pickett, Poppy, Powell, Wadhams and Woodcock2001). The aim of the present study is to assess whether P. humuli is inhibited from colonizing hop plants sprayed with (Z)-jasmone, as might be inferred by the negative response of several other aphid species to secondary host-plants sprayed with this compound.
Materials and methods
Randomized complete block experiments were conducted in plantations of dwarf hops, Humulus lupulus (L.), at East Malling Research in 2002 and 2003. Hops were grown in 30 m rows consisting of six 5 m panels and the hop stems (bines) were supported by a 2.4 m high trellis. The second and fifth panel formed the individual plots in each block. Three of the six blocks were on cv. Herald and three on cv. First Gold.
(Z)-Jasmone (Sigma-Aldrich, UK; purity 90%) was applied to all hop plants in a panel using an Oxford Precision Sprayer (MDM Engineering Ltd, UK) fitted with a fan nozzle (015 F110). Each treatment panel was sprayed with 0.125 g (Z)-jasmone solubilized in 0.5 l of water by means of a non-ionic surfactant (Ethylan BV, Akcros Chemicals, UK, 0.1%), which is equivalent to 50 g (Z)-jasmone ha−1. The control used the same formulation, minus the (Z)-jasmone, applied at the same rate. Random numbers were used to select which of the two panels received the (Z) Jasmone and which the control, in each block.
Six healthy hop bines in the centre of each hop panel were selected for aphid assessments. Twenty-four hours after treatment applications all spring migrants on the three apical leaf pairs on each of the bines were counted and removed. Thereafter, numbers of spring migrants were counted and removed daily. Aphid numbers were recorded between 1–15 June 2002, and 12–21 June 2003. In order to reduce the risk of missing transient effects from treating hop plants with (Z)-jasmone, each recording period was divided into five-day blocks.
Data were examined by analysis of variance (ANOVA) using GenStat 5 (Payne, Reference Payne2000). In order to stabilize variances, the daily counts were transformed to square roots (n0.5) and summed across three sampling periods, 2–6 days, 7–11 days and 12–16 days, after treatment application in 2002 and over the first two sampling periods in 2003.
Results and discussion
A total of 7461 P. humuli spring migrants was removed from assessed hop bines in 2002 and 610 in 2003 (table 1). In the first five-day period after treatment, significantly more spring migrants were removed from hop bines treated with (Z)-jasmone than controls in 2002 (F 1,5=23.91, P=0.05). However, that pattern was reversed in the second and third five-day sampling periods, but the differences were non-significant.
Total numbers of Phorodon humuli spring migrants removed from hop bines during five-day periods after spraying the plants with (Z)-jasmone in 2002 and 2003.
A similar increase in aphids on the treated plants was observed in 2003. However, because the migration to hop was much lighter than in 2002, the difference failed to achieve statistical significance by ANOVA in either five-day sampling period (although a contingency test between totals on treated and untreated bines in 2003 was significant; χ2=8.03, P<0.01). Indeed, more spring migrants were removed from bines treated with (Z)-jasmone than from untreated bines in the first and second five-day periods (11 and 44%, respectively) in 2003. By contrast, greater numbers (23%) of aphids were removed from treated bines only in the first five-day period in 2002.
Jasmonic acid and its methyl ester are known to stimulate production of various defence-related secondary metabolites by plants in response to stress, such as attack by insect herbivores (Blechert et al., Reference Blechert, Brodschelm, Hölder, Kammerer, Kutchan, Mueller, Xia and Zenk1995). Furthermore, because methyl jasmonate is volatile, it can act as an airborne signal for such processes (Farmer & Ryan, Reference Farmer and Ryan1990). Birkett et al. (Reference Birkett, Campbell, Chamberlain, Guerrieri, Hick, Martin, Matthes, Napier, Pickett, Poppy, Pow, Pye, Smart, Wadhams, Wadhams and Woodcock2000) and Bruce et al. (Reference Bruce, Martin, Pickett, Pye, Smart and Wadhams2003) found that the biosynthetically related (Z)-jasmone is also involved in plant defence responses. In olfactometer studies, the aphids N. ribis-nigri (Birkett et al., Reference Birkett, Campbell, Chamberlain, Guerrieri, Hick, Martin, Matthes, Napier, Pickett, Poppy, Pow, Pye, Smart, Wadhams, Wadhams and Woodcock2000) and S. avenae (Bruce et al., Reference Bruce, Martin, Pickett, Pye, Smart and Wadhams2003) responded negatively to (Z)-jasmone, and sprays of the compound significantly reduced numbers of colonizing cereal aphids on plants treated with (Z)-jasmone.
By contrast, although traps releasing (Z)-jasmone caught significantly fewer P. humuli spring migrants than controls (Birkett et al., Reference Birkett, Campbell, Chamberlain, Guerrieri, Hick, Martin, Matthes, Napier, Pickett, Poppy, Pow, Pye, Smart, Wadhams, Wadhams and Woodcock2000), spraying the chemical on hop plants increased the numbers that settled on the treated plants. However, as (Z)-jasmone is highly volatile (Koch et al., Reference Koch, Bandemer and Boland1997), it is unlikely to have remained on the surface of the hop plants for long. Therefore, the results presented here are more likely due to the effects that (Z)-jasmone has on hops rather than to any direct effects of this compound on the behaviour of P. humuli spring migrants.
Bean plants appear to selectively take up (Z)-jasmone from the aerial phase (Chamberlain et al., Reference Chamberlain, Guerrieri, Pennacchio, Pettersson, Pickett, Poppy, Powell, Wadhams and Woodcock2001), which may have resulted in the plants producing increased levels of compounds associated with insect damage (Birkett et al., Reference Birkett, Campbell, Chamberlain, Guerrieri, Hick, Martin, Matthes, Napier, Pickett, Poppy, Pow, Pye, Smart, Wadhams, Wadhams and Woodcock2000). It is possible that (Z)-jasmone is also selectively taken up by hop plants and that this results in changes to the volatile profile produced by treated plants. Interestingly, changes to the volatile profile of bean plants treated with (Z)-jasmone lasted eight days (Birkett et al., Reference Birkett, Campbell, Chamberlain, Guerrieri, Hick, Martin, Matthes, Napier, Pickett, Poppy, Pow, Pye, Smart, Wadhams, Wadhams and Woodcock2000). Similarly, in the present study, a significant difference in numbers of P. humuli spring migrants removed from hop bines was only recorded for the first five-day period after applying (Z)-jasmone in 2002. Further work is required to determine the effects of (Z)-jasmone on the volatiles produced by hop plants and, subsequently, to test the responses of spring migrants to these compounds.
Phorodon humuli spring migrants appear to respond positively to hop plants sprayed with (Z)-jasmone, which contrasts with the negative response of cereal aphids to winter wheat similarly sprayed with (Z)-jasmone (Birkett et al., Reference Birkett, Campbell, Chamberlain, Guerrieri, Hick, Martin, Matthes, Napier, Pickett, Poppy, Pow, Pye, Smart, Wadhams, Wadhams and Woodcock2000; Bruce et al., Reference Bruce, Martin, Pickett, Pye, Smart and Wadhams2003). This may reflect the fact that P. humuli frequently over-exploits hop plants (Barber et al., Reference Barber, Campbell, Crane, Darby and Lilley2003) unlike some aphid species; Myzus persicae (Sulzer) (Hemiptera: Aphididae), for example, characteristically occurs in sparse populations. For M. persicae, spacing out behaviour, sensitivity to food plant quality and ready induction of dispersive winged morphs in response to moderate crowding ensures that populations mostly remain at low densities (Way & Cammell, Reference Way, Cammell, den Boer and Gradwell1970). However, in P. humuli inherent qualities and dispersal behaviour are less effective at regulating populations, which allows a build-up to excessive and destructive numbers.
Acknowledgements
T.W.P. was funded by the East Malling Trust for Horticultural Research and C.A.M.C. by the Department for Environment Food and Rural Affairs. J.H. was funded by the Biotechnology and Biological Sciences Research Council (BBSRC). Rothamsted Research receives grant-aided support from the BBSRC.
