Mini-review Received: 9 June 2014
Revised: 22 September 2014
Accepted article published: 25 September 2014
Published online in Wiley Online Library:
(wileyonlinelibrary.com) DOI 10.1002/ps.3915
The push–pull strategy for citrus psyllid control Huaxue Yan,a,b,c Jiwu Zenga,b,c and Guangyan Zhonga,b,c* Abstract The Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is the only natural vector of Candidatus Liberibacter asiaticus that causes citrus huanglongbing (HLB), a most destructive disease of citrus. Currently, no remedial therapy exists for the disease, and so effective control of ACP is very important in curbing the transmission of the disease. The push–pull strategy should be thoroughly explored as an approach to ACP management. This mini-review summarises the current progress towards more effective repellent and attractant chemicals through investigating known repellent and attractive plants. Interactions between ACP and its host plants are also addressed, with emphasis on the possible involvement of the host biochemicals in attracting the insect. Potential ways to increase the effectiveness of the pull–push strategy are briefly discussed. It is expected that the pull–push strategy will be gradually developed following more extensive research. © 2014 Society of Chemical Industry Keywords: citrus psyllid; attractant; repellent; push–pull strategy
1
INTRODUCTION
The citrus psyllid transmits citrus huanglongbing (HLB), the world’s most devastating disease of Citrus, by serving as a vector for the disease causal agents Candidatus liberibacter spp. (Alphaproteobacteria). Species of psyllid involved include Diaphorina citri (the Asian citrus psyllid, ACP) in Asia and America, and Trioza erytreae in Africa.1 ACP and HLB have spread rapidly to citrus-growing regions worldwide, especially in the last decade. They have been found in North and South American countries, including Mexico, Brazil, the United States, Belize, Costa Rica, Cuba, Guatemala, Honduras, Jamaica, Nicaragua and Dominican Republic,2 and in a number of countries in Asia and Africa. In China, HLB has been reported from 11 citrus-growing provinces.3 In the United States, HLB spread to all Florida citrus-producing counties between 2004 and 2012, and Florida’s citrus acreage has consequently shrunk by about a third.4 HLB causes yellow shoots, leaf mottling and chlorosis (resembling zinc deficiency), twig dieback, reduced fruit size and quality and eventually tree death.5 Practically all commercial citrus species and cultivars are sensitive to the disease, and currently there is no cure for it.1 It is difficult to manage HLB within its current geographic range and to curb its transmission to new areas. This is because the disease’s vector, ACP, can multiply and spread HLB throughout the year in most major citrus-growing areas. Intensive chemical control of ACP with foliar and systemic insecticides (e.g. imidacloprid, fenpropathrin, chlorpyrifos and dimethoate) is considered to be effective in reducing citrus psyllid populations in many areas.6 – 10 However, insecticides by nature are costly and unsustainable. They are also ineffective at preventing the spread of HLB to new citrus plantings.9,11 Biological control agents include native predators12 and an exotic parasitoid,13 and are not very effective. These, however, are not management options once a grove is infected by HLB.14,15 Novel and sustainable approaches to controlling ACP are urgently needed. In this respect, the behavioural control strategy known as stimulodeterrent diversion16 or push–pull strategy17 has attracted increasing Pest Manag Sci (2014)
attention. This review looks at recent advances in attractant and repellent research, and the possibility of a push–pull strategy for ACP management.
2
PUSH–PULL STRATEGY
The push–pull or stimulodeterrent diversion strategy of pest management was developed independently by Pyke et al. for Helicoverpa spp.18 and by Miller and Cowles for Delia antiqua.16 In the strategy, pest insects are either repelled or deterred away from the resource (push) by using stimuli that repel the insects or mask the host, or attracted (pull) to other areas by using stimuli that lure the insects.17 Push components include visual cues, synthetic repellents, non-host volatiles, host-derived semiochemicals, antiaggregation pheromones, alarm pheromones, antifeedants, egg laying deterrents and deterrent pheromones. Pull components consist of visual stimulants, host volatiles, sex pheromones, aggregation pheromones, gustatory stimulants and egg laying stimulants.17 As push–pull chemicals are generally non-toxic, the strategy is environmentally friendly. For example, combining the application of neem seed extracts to the main crop (push), with the use of an attractive crop (pull) of either pigeon pea (Cajanus cajan) or maize (Zea mays), has successfully protected cotton (Gossypium hirsutum) from Helicoverpa armigera and H. punctigera.18,19 ACP repellents based on plant volatiles or
∗
Correspondence to: Guangyan Zhong, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, China E-mail: [email protected]
a Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, China b Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilisation, Ministry of Agriculture, Guangzhou, China c Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Guangzhou, China
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H Yan, J Zeng and G Zhong
plant-derived essential oils have been suggested.20,21 Studies on how ACP is attracted to its natural hosts (Rutaceae plants) are ongoing,22 which could lead to the development and application of a usable push–pull system for the control of this pest in the near future.
and thyme inhibited the visitation of ACP when copresented with citrus leaves, but the primary volatiles present in coriander oil (𝛼-pinene and linalool) did not repel ACP adults compared with clean air.29 When calamondin orange leaves were paired with leaves of guava, billygoat weed or green leaf desmodium, the presence of volatiles from these plants reduced feeding of the psyllid adults on calamondin, suggesting that understories of billygoat weed or desmodium in orchards may reduce feeding and egg laying of ACP and may thus have practical implications in ACP management in orchards.26
3
PSYLLID REPELLENT RESEARCH
Physical repellents, such as clay particle film and metallised polyethylene mulch, have reduced the spread of ACP, but both need further evaluation.23 – 25 The suppressive effect of the clay particle film against adult psyllid was attributed to its inhibition of the ability of the adult to grasp, move and oviposit on leaves, but the thin film can be easily washed off by rain or ruptured by expanding leaves and elongating shoots.23 It was reported that metallised mulch slowed down the spread of HLB on young citrus trees and increased tree growth rate, thus shortening the time to crop profitability.25 Research suggests that chemical repellents, including horticultural mineral oils (HMOs) and noxious plant products, could be used in ACP management.7,10 HMOs work by suppressing attractant plant volatiles, releasing repellent volatiles and reducing the number of eggs deposited.10,26 However, different HMOs differ significantly in their repelling capacity against ACP.27 Some HMOs are highly effective on ACP, but their practical use is still under development.28,29 Repellents based on plant volatiles have attracted some attention since 2004, when a unique interaction between citrus and guava, Psidium guajava L., was found in Vietnam.30 There, when planted alone, citrus trees survived usually only for 2–4 years before being easily infected with HLB, but they could survive for up to 15 years when interplanted with white guava. Later research showed that the population of ACP was reduced to nearly undetectable levels in interplantings (compared with monocultures) in Japan and Australia.30 The repellent effect of guava leaves against adult psyllids was assumed to come from some volatile compounds rather than physical factors, as both young and old guava leaves showed equal repelling activity.21 Newly published research shows that, although no citrus trees in orchards interplanted with guavas were infected by HLB in the first year, about 20% of the trees without guavas interplanted were infected. However, the repellent effect did not last long because almost all trees intercropped with guavas were infected with HLB after two and a half years.31 A GC-MS study of the volatiles from crushed and intact guava leaves (P. guajava L.) and citrus leaves showed that dimethyl disulfide (DMDS) might be the component responsible for the repellent effect, and it was noted that the volatile was produced by wounded guava leaves but not by citrus leaves.32 The assumption was verified when a field deployment of DMDS resulted in reduced densities of ACP.33 Plant volatiles from garlic chive (Allium tuberosum Rottl.) inhibited the response of ACP to citrus volatiles, but did not affect the behaviour of the pest’s ectoparasitoid Tamarixia radiata (Waterston).28 Analysis of the headspace components of crushed garlic chive leaves and the garlic chive essential oil by GC-MS revealed that it was the primary sulfur volatiles (disulfides and trisulfides) that inhibited the response of ACP to citrus volatiles.28 Other plants were investigated for their repellent effect on ACP. In a study of the taxis of ACP to the volatile oils extracted from non-host plants, volatiles from Mikania micrantha, Lantana camera, Eupatorium catarium and Wedelia chinensis significantly reduced the number of ACP adults.20 Oils from coriander, lavender, rose
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4
PSYLLID ATTRACTANT RESEARCH
ACP is oligophagous on rutaceous host plants. The preference of ACP for different Rutaceae species has been investigated.22,34,35 Research has shown that stimuli (visual and olfactory) emitted by flushing shoots play an important role in the detection, location and evaluation of potential host plants by ACP.36 ACP is attracted to the bright-yellow and green visual cues that are indicative of flushing shoots.36 The insect may mate, oviposit and develop exclusively on new flush shoots.37,38 A few ACPs can be trapped by yellow glue board.39 In a study on the population dynamics of ACP in orchards of ‘Valencia’ orange, ‘Ponkan’ mandarin and ‘Murcott’ tangor trees, yellow sticky traps were used to monitor the insect.40 ACP responded to the odour of several host plants in a Y-tube olfactometer by detecting foliar volatiles with its antennae.36 Citrus paradisii (grapefruit) was the most preferred host relative to Murraya paniculata (orange jasmine), C. jambhiri (rough lemon) and C. aurantium (sour orange).41 More adults selected C. suhuiensis than M. paniculata.35 In Zhejiang, China, the preferred hosts of ACP were commercial citrus, followed by M. paniculata and Poncirus trifoliata.15 Host flush growth stages and volatile compounds affected egg laying and feeding site selection of ACP, and more ACP adults were attracted to plants with newly expanded leaves for egg laying and feeding.35 The presence of visual cues enhanced the attractiveness of olfactory cues, and ACP showed strong evidence of attraction only when olfactory and visual cues coexisted.36 ACP population densities in citrus groves were much lower than in M. paniculata hedges in the northern distribution areas of the insect in Japan. This may be due to the continuous production of new shoots in dense plantings of M. paniculata hedges, favouring the reproduction and survival of ACP.42 It has also been noted that male and female ACPs responded differentially to host plant odour.34 Both males and females preferred the odour from the young shoots of M. paniculata (L.) Jack and C. limon (L.) Burm. F. cv. Eureka. Only males preferred the odour of C. sinensis (L.), whereas the odour of Citrus paradisii (MacFadyen cv. Rio Red) was attractive to neither sex. A mixture of synthetic terpenes, modelled on the volatiles collected from M. paniculata, was attractive.34 Responses of ACP to volatiles emitted by its rutaceous host plants varied with mating status, as attraction was stronger to females and to mated individuals of both sexes than to virgins.36 ACP responded differently to the odour emitted by its host plants. When the host trees were infected by Candidatus Liberibacter asiaticus (CLas), the number of adults and eggs on symptomatic shoots was significantly higher than on non-symptomatic shoots.43 Although CLas-infected plants were initially more attractive to ACP adults than were non-infected plants, the non-infected healthy plants were preferred settling points for the dispersing psyllids after being contracted with HLB bacteria from feeding on diseased trees.44 It is
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Pest Manag Sci (2014)
The push-pull strategy for citrus psyllid control
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believed that CLas-infected citrus plants attracted adult ACP by altering leaf colour, headspace volatiles and plant nutritional contents.44 A GC-MS analysis of volatiles showed that (+)-epi-bicyclosesquiphellandrene was only detected in CLas-infected shoots, but ocimene, germacrene D, 𝛿-cadinene, d-longifolene and 𝛼-sinensal were detected only in healthy shoots.43 Metabolomic differentiation of HLB-infected, zinc-deficient and healthy leaves of ‘Valencia’ sweet orange revealed that proline, 𝛽-elemene, (−)trans-caryophyllene and 𝛼-humulenewere possible biomarkers for HLB.45 Significantly more methyl salicylate and less methyl anthranilate and D-limonene were released by infected plants than by non-infected plants, and feeding on citrus by ACP adults also induced the release of methyl salicylate. Methyl salicylate was attractive to ACP, while methyl anthranilate was not.44 The volatile profiles of the young leaves of six Rutaceae species were analysed in relation to the attractiveness of these species to ACP, which varied from highest to lowest as shown by the infested number of ACPs on them: Bergera koenigii (L.) (curry leaf tree), M. paniculata (L.) Jack (orange jasmine), C. macrophylla Wester, C. sinensis (L.) Osbeck ‘Valencia’, C. jambhiri Lush. (‘Rough’ lemon) and P. trifoliata (L.) (trifoliate orange).22 The results suggested a subset of likely candidate chemicals for evaluation in behavioural assays. For example, high concentrations of sabinene and 𝛽-phellandrene were found in attractive genotypes of C. sinensis (L.) Osbeck ‘Valencia’ and B. koenigii (L.) respectively, whereas large amounts of limonene were found in less attractive genotypes of C. jambhiri Lush. (‘Rough’ lemon) and C. macrophylla Wester.
5 WORK WITH OTHER INSECTS MAY PROVIDE CLUES FOR ACP REPELLENT RESEARCH DMDS has been reported as being repellent to other insects. The non-lethal repellent action of DMDS against adult mirid bug, Apolygus lucorum (a major pest of cotton, fruit trees and many other crops), was demonstrated under laboratory and field conditions.46 DMDS at a certain range of doses showed a significant repellent effect on potato psyllid, Bactericera cockerelli (Sulc), and it remained repellent during the whole 10 day longevity residual trial.47 𝛼-Pinene has repellent and toxic effects on the grain-storage insects Sitophilus zeamais, Rhyzopetha dominica and Tribolium castaneum.48 𝛽-Pinene has a repellent effect on grain moth Sitotroga cereallela.49 The response of Cryptomeria bark borer to the essential oil of Japanese cedar (Cryptomeria japonica D. Don) and its components was studied, and high repellent activity to Cryptomeria bark borer was shown by 𝛼-terpineol, nerolidol, 𝛿-cadinene and 𝛽-eudesmol of the oil.50 The sesquiterpene (E)-𝛽-farnesene was repellent to the pea aphid, Acyrthosiphon pisum (Harr), and the grain aphid, Sitobion avenae F.51 The feeding and egg laying of the carrot psyllid, Trioza apicalis, were reduced by application of fresh spruce and pine sawdust along the seedling rows in carrot fields.52 Recent research on the tritrophic system of pear trees, psyllid herbivores and anthocorid predators has indicated that the insects are highly attracted to methyl salicylate, possibly because infested pear trees are characterised by the odour of the chemical.53 Not coincidentally, feeding on citrus by ACP adults also induced release of methyl salicylate.44 These results suggest that methyl salicylate could be used practically as an attractant for psyllids. Pest Manag Sci (2014)
6 IS THE PUSH–PULL STRATEGY APPLICABLE IN CITRUS PSYLLID CONTROL? Effective control of ACP is an important component in a successful HLB management programme.25 In this regard, the push–pull strategy should be explored experimentally, as the method has potential to offer not only efficient control of ACP populations but also less significant adverse effects on the environment. Signs have been accumulating that the strategy works practically. As already mentioned, habitat diversification by intercropping citrus with guava showed a good effect on repelling ACP, although the efficacy varied in different studies. The currently known chemicals from limited studies on repellent plants have yet to be put into use in the field, but they can be chemically modified to be more effective. In addition, more effective chemicals may also be discovered if more repellent plants are investigated. Chemicals in volatiles of ACP host plants are similarly promising if used as attractants after chemical modification or used in combination after formulating the best of them together. In addition, modern genetics may be a pathway to modifying the host plants so that they will no longer be attractive to ACP. Before a practical pull–push method can be developed, a deeper knowledge of the behaviour of ACP and the interactions of this insect with its host plants is needed.
ACKNOWLEDGEMENT This work was supported by the International Science and Technology Cooperation Programme of China (Grant No. 2012DFA30610) and the Science and Technology Planning Project of Guangdong Province (Grant No. 2012A020200016).
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citri Kuwayama to host plant volatiles. J Appl Entomol 135:404–414 (2011). Patt JM and Sétamou M, Responses of the Asian citrus psyllid to volatiles emitted by the flushing shoots of its rutaceous host plants. Environ Entomol 39:618–624 (2010). Sule H, Muhamad R, Omar D and Hee AKW, Response of Diaphorina citri Kuwayama (Hemiptera: Psyllidae) to volatiles emitted from leaves of two rutaceous plants. J Agric Sci 4:152–159 (2012). Wenninger EJ, Stelinski LL and Hall DG, Roles of olfactory cues, visual cues, and mating status in orientation of Diaphorina citri Kuwayama (Hemiptera: Psyllidae) to four different host plants. Environ Entomol 38:225–234 (2009). Moran VC and Buchan PR, Oviposition by the citrus psylla, Trioza erytreae (Homoptera: Psyllidae), in relation to leaf hardness. Entomol Exp Applic 18:96–104 (1975). Hall DG and Albrigo LG, Estimating the relative abundance of flush shoots in citrus with implications on monitoring insects associated with flush. HortScience 42:364–368 (2007). Deng M, Chen G, Tang M, Chen T, Tan Y and Li S, Field trial preliminary of trapping adult citrus psylla with yellow trap (Abstract in English). Chin Agric Sci Bull 26:247–251 (2010). Beloti VH, Rugno GR, Felippe MR, Carmo-Uehara AD, Garbim LF, Godoy WA et al., Population dynamics of Diaphorina citri Kuwayama (Hemiptera: Liviidae) in orchards of ‘Valencia’ orange, ‘Ponkan’ mandarin and ‘Murcott’ tangor trees. Fla Entomol 96:173–179 (2013). Tsai JH and Liu YH, Biology of Diaphorina citri (Homoptera: Psyllidae) on four host plants. J Econ Entomol 93:1721–1725 (2000). Ikeda K and Ashihara W, Preference of adult Asian citrus psyllid, Diaphorina citri (Homoptera: Psyllidae), for Murraya paniculata and Citrus unshiu. Jap J Appl Entomol Zool 52:27–30 (2008). Zhao JP, Wang HT, Zeng XN and Xue PP, Differences in selection behaviors and chemical cues of adult Asian citrus psyllids, Diaphorina citri, on healthy and huanglongbing-infected young shoots of citrus plants. J Agric Sci 5:83–91 (2013). Mann RS, Ali JG, Hermann SL, Tiwari S, Pelz-Stelinski KS, Alborn HT et al., Induced release of a plant-defense volatile ‘deceptively’ attracts insect vectors to plants infected with a bacterial pathogen. PLoS Pathog 8(3):e1002610 (2012). Cevallos-Cevallos JM, García-Torres R, Etxeberria E and Reyes-De-Corcuera JI, GC-MS analysis of headspace and liquid extracts for metabolomic differentiation of citrus huanglongbing and zinc deficiency in leaves of ‘Valencia’ sweet orange from commercial grove. Phytochem Anal 22:236–246 (2011). Pan H, Lu Y and Wyckhuy AK, Repellency of dimethyl disulfide to Apolygus lucorum (Meyer-Dür) (Hemiptera: Miridae) under laboratory and field conditions. Crop Prot 50:40–45 (2013). Diaz-Montano J and Trumble JT, Behavioral responses of the potato psyllid (Hemiptera: Triozidae) to volatiles from dimethyl disulfide and plant essential oils. J Insect Behav 26:336–351 (2013). Huang F, Zheng J, Zhang L, Ma T, Chen Y and Xiao G, Research on the protection of stored grain from pest by 𝛼-pinene (Abstract in English). Grain Stor 17:34–43 (1988). Krishnarajah SR, Ganesalingam VK and Senanayake UM, Repellancy and toxicity of some plant oils and their terpene components to Sitotroga cerealella (Olivier), (Lepidoptera, Gelechiidae). Trop Sci 25:249–252 (1985). Yatagai M, Makihara H and Oba K, Volatile components of Japanese cedar cultivars as repellents related to resistance to Cryptomeria bark borer. J Wood Sci 48:51–55 (2002). Bruce TJA, Birkett MA, Blande J, Hooper AM, Martin JL, Khambay B et al., Response of economically important aphids to components of Hemizygia petiolata essential oil. Pest Manag Sci 61:1115–1121 (2005). Nehlin G, Valterová I and Borg-Karlson AK, Use of conifer volatiles to reduce injury caused by carrot psyllid, Trioza apicalis, Förster (Homoptera, Psylloidea). J Chem Ecol 20:771–783 (1994). Molleman F, Drukker B and Blommers L, A trap for monitoring pear psylla predators using dispensers with the synomone methylsalicylate. Proc Exp Applic Entomol 8:177–182 (1997).
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© 2014 Society of Chemical Industry
Pest Manag Sci (2014)
Revised: 22 September 2014
Accepted article published: 25 September 2014
Published online in Wiley Online Library:
(wileyonlinelibrary.com) DOI 10.1002/ps.3915
The push–pull strategy for citrus psyllid control Huaxue Yan,a,b,c Jiwu Zenga,b,c and Guangyan Zhonga,b,c* Abstract The Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is the only natural vector of Candidatus Liberibacter asiaticus that causes citrus huanglongbing (HLB), a most destructive disease of citrus. Currently, no remedial therapy exists for the disease, and so effective control of ACP is very important in curbing the transmission of the disease. The push–pull strategy should be thoroughly explored as an approach to ACP management. This mini-review summarises the current progress towards more effective repellent and attractant chemicals through investigating known repellent and attractive plants. Interactions between ACP and its host plants are also addressed, with emphasis on the possible involvement of the host biochemicals in attracting the insect. Potential ways to increase the effectiveness of the pull–push strategy are briefly discussed. It is expected that the pull–push strategy will be gradually developed following more extensive research. © 2014 Society of Chemical Industry Keywords: citrus psyllid; attractant; repellent; push–pull strategy
1
INTRODUCTION
The citrus psyllid transmits citrus huanglongbing (HLB), the world’s most devastating disease of Citrus, by serving as a vector for the disease causal agents Candidatus liberibacter spp. (Alphaproteobacteria). Species of psyllid involved include Diaphorina citri (the Asian citrus psyllid, ACP) in Asia and America, and Trioza erytreae in Africa.1 ACP and HLB have spread rapidly to citrus-growing regions worldwide, especially in the last decade. They have been found in North and South American countries, including Mexico, Brazil, the United States, Belize, Costa Rica, Cuba, Guatemala, Honduras, Jamaica, Nicaragua and Dominican Republic,2 and in a number of countries in Asia and Africa. In China, HLB has been reported from 11 citrus-growing provinces.3 In the United States, HLB spread to all Florida citrus-producing counties between 2004 and 2012, and Florida’s citrus acreage has consequently shrunk by about a third.4 HLB causes yellow shoots, leaf mottling and chlorosis (resembling zinc deficiency), twig dieback, reduced fruit size and quality and eventually tree death.5 Practically all commercial citrus species and cultivars are sensitive to the disease, and currently there is no cure for it.1 It is difficult to manage HLB within its current geographic range and to curb its transmission to new areas. This is because the disease’s vector, ACP, can multiply and spread HLB throughout the year in most major citrus-growing areas. Intensive chemical control of ACP with foliar and systemic insecticides (e.g. imidacloprid, fenpropathrin, chlorpyrifos and dimethoate) is considered to be effective in reducing citrus psyllid populations in many areas.6 – 10 However, insecticides by nature are costly and unsustainable. They are also ineffective at preventing the spread of HLB to new citrus plantings.9,11 Biological control agents include native predators12 and an exotic parasitoid,13 and are not very effective. These, however, are not management options once a grove is infected by HLB.14,15 Novel and sustainable approaches to controlling ACP are urgently needed. In this respect, the behavioural control strategy known as stimulodeterrent diversion16 or push–pull strategy17 has attracted increasing Pest Manag Sci (2014)
attention. This review looks at recent advances in attractant and repellent research, and the possibility of a push–pull strategy for ACP management.
2
PUSH–PULL STRATEGY
The push–pull or stimulodeterrent diversion strategy of pest management was developed independently by Pyke et al. for Helicoverpa spp.18 and by Miller and Cowles for Delia antiqua.16 In the strategy, pest insects are either repelled or deterred away from the resource (push) by using stimuli that repel the insects or mask the host, or attracted (pull) to other areas by using stimuli that lure the insects.17 Push components include visual cues, synthetic repellents, non-host volatiles, host-derived semiochemicals, antiaggregation pheromones, alarm pheromones, antifeedants, egg laying deterrents and deterrent pheromones. Pull components consist of visual stimulants, host volatiles, sex pheromones, aggregation pheromones, gustatory stimulants and egg laying stimulants.17 As push–pull chemicals are generally non-toxic, the strategy is environmentally friendly. For example, combining the application of neem seed extracts to the main crop (push), with the use of an attractive crop (pull) of either pigeon pea (Cajanus cajan) or maize (Zea mays), has successfully protected cotton (Gossypium hirsutum) from Helicoverpa armigera and H. punctigera.18,19 ACP repellents based on plant volatiles or
∗
Correspondence to: Guangyan Zhong, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, China E-mail: [email protected]
a Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, China b Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilisation, Ministry of Agriculture, Guangzhou, China c Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Guangzhou, China
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H Yan, J Zeng and G Zhong
plant-derived essential oils have been suggested.20,21 Studies on how ACP is attracted to its natural hosts (Rutaceae plants) are ongoing,22 which could lead to the development and application of a usable push–pull system for the control of this pest in the near future.
and thyme inhibited the visitation of ACP when copresented with citrus leaves, but the primary volatiles present in coriander oil (𝛼-pinene and linalool) did not repel ACP adults compared with clean air.29 When calamondin orange leaves were paired with leaves of guava, billygoat weed or green leaf desmodium, the presence of volatiles from these plants reduced feeding of the psyllid adults on calamondin, suggesting that understories of billygoat weed or desmodium in orchards may reduce feeding and egg laying of ACP and may thus have practical implications in ACP management in orchards.26
3
PSYLLID REPELLENT RESEARCH
Physical repellents, such as clay particle film and metallised polyethylene mulch, have reduced the spread of ACP, but both need further evaluation.23 – 25 The suppressive effect of the clay particle film against adult psyllid was attributed to its inhibition of the ability of the adult to grasp, move and oviposit on leaves, but the thin film can be easily washed off by rain or ruptured by expanding leaves and elongating shoots.23 It was reported that metallised mulch slowed down the spread of HLB on young citrus trees and increased tree growth rate, thus shortening the time to crop profitability.25 Research suggests that chemical repellents, including horticultural mineral oils (HMOs) and noxious plant products, could be used in ACP management.7,10 HMOs work by suppressing attractant plant volatiles, releasing repellent volatiles and reducing the number of eggs deposited.10,26 However, different HMOs differ significantly in their repelling capacity against ACP.27 Some HMOs are highly effective on ACP, but their practical use is still under development.28,29 Repellents based on plant volatiles have attracted some attention since 2004, when a unique interaction between citrus and guava, Psidium guajava L., was found in Vietnam.30 There, when planted alone, citrus trees survived usually only for 2–4 years before being easily infected with HLB, but they could survive for up to 15 years when interplanted with white guava. Later research showed that the population of ACP was reduced to nearly undetectable levels in interplantings (compared with monocultures) in Japan and Australia.30 The repellent effect of guava leaves against adult psyllids was assumed to come from some volatile compounds rather than physical factors, as both young and old guava leaves showed equal repelling activity.21 Newly published research shows that, although no citrus trees in orchards interplanted with guavas were infected by HLB in the first year, about 20% of the trees without guavas interplanted were infected. However, the repellent effect did not last long because almost all trees intercropped with guavas were infected with HLB after two and a half years.31 A GC-MS study of the volatiles from crushed and intact guava leaves (P. guajava L.) and citrus leaves showed that dimethyl disulfide (DMDS) might be the component responsible for the repellent effect, and it was noted that the volatile was produced by wounded guava leaves but not by citrus leaves.32 The assumption was verified when a field deployment of DMDS resulted in reduced densities of ACP.33 Plant volatiles from garlic chive (Allium tuberosum Rottl.) inhibited the response of ACP to citrus volatiles, but did not affect the behaviour of the pest’s ectoparasitoid Tamarixia radiata (Waterston).28 Analysis of the headspace components of crushed garlic chive leaves and the garlic chive essential oil by GC-MS revealed that it was the primary sulfur volatiles (disulfides and trisulfides) that inhibited the response of ACP to citrus volatiles.28 Other plants were investigated for their repellent effect on ACP. In a study of the taxis of ACP to the volatile oils extracted from non-host plants, volatiles from Mikania micrantha, Lantana camera, Eupatorium catarium and Wedelia chinensis significantly reduced the number of ACP adults.20 Oils from coriander, lavender, rose
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4
PSYLLID ATTRACTANT RESEARCH
ACP is oligophagous on rutaceous host plants. The preference of ACP for different Rutaceae species has been investigated.22,34,35 Research has shown that stimuli (visual and olfactory) emitted by flushing shoots play an important role in the detection, location and evaluation of potential host plants by ACP.36 ACP is attracted to the bright-yellow and green visual cues that are indicative of flushing shoots.36 The insect may mate, oviposit and develop exclusively on new flush shoots.37,38 A few ACPs can be trapped by yellow glue board.39 In a study on the population dynamics of ACP in orchards of ‘Valencia’ orange, ‘Ponkan’ mandarin and ‘Murcott’ tangor trees, yellow sticky traps were used to monitor the insect.40 ACP responded to the odour of several host plants in a Y-tube olfactometer by detecting foliar volatiles with its antennae.36 Citrus paradisii (grapefruit) was the most preferred host relative to Murraya paniculata (orange jasmine), C. jambhiri (rough lemon) and C. aurantium (sour orange).41 More adults selected C. suhuiensis than M. paniculata.35 In Zhejiang, China, the preferred hosts of ACP were commercial citrus, followed by M. paniculata and Poncirus trifoliata.15 Host flush growth stages and volatile compounds affected egg laying and feeding site selection of ACP, and more ACP adults were attracted to plants with newly expanded leaves for egg laying and feeding.35 The presence of visual cues enhanced the attractiveness of olfactory cues, and ACP showed strong evidence of attraction only when olfactory and visual cues coexisted.36 ACP population densities in citrus groves were much lower than in M. paniculata hedges in the northern distribution areas of the insect in Japan. This may be due to the continuous production of new shoots in dense plantings of M. paniculata hedges, favouring the reproduction and survival of ACP.42 It has also been noted that male and female ACPs responded differentially to host plant odour.34 Both males and females preferred the odour from the young shoots of M. paniculata (L.) Jack and C. limon (L.) Burm. F. cv. Eureka. Only males preferred the odour of C. sinensis (L.), whereas the odour of Citrus paradisii (MacFadyen cv. Rio Red) was attractive to neither sex. A mixture of synthetic terpenes, modelled on the volatiles collected from M. paniculata, was attractive.34 Responses of ACP to volatiles emitted by its rutaceous host plants varied with mating status, as attraction was stronger to females and to mated individuals of both sexes than to virgins.36 ACP responded differently to the odour emitted by its host plants. When the host trees were infected by Candidatus Liberibacter asiaticus (CLas), the number of adults and eggs on symptomatic shoots was significantly higher than on non-symptomatic shoots.43 Although CLas-infected plants were initially more attractive to ACP adults than were non-infected plants, the non-infected healthy plants were preferred settling points for the dispersing psyllids after being contracted with HLB bacteria from feeding on diseased trees.44 It is
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Pest Manag Sci (2014)
The push-pull strategy for citrus psyllid control
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believed that CLas-infected citrus plants attracted adult ACP by altering leaf colour, headspace volatiles and plant nutritional contents.44 A GC-MS analysis of volatiles showed that (+)-epi-bicyclosesquiphellandrene was only detected in CLas-infected shoots, but ocimene, germacrene D, 𝛿-cadinene, d-longifolene and 𝛼-sinensal were detected only in healthy shoots.43 Metabolomic differentiation of HLB-infected, zinc-deficient and healthy leaves of ‘Valencia’ sweet orange revealed that proline, 𝛽-elemene, (−)trans-caryophyllene and 𝛼-humulenewere possible biomarkers for HLB.45 Significantly more methyl salicylate and less methyl anthranilate and D-limonene were released by infected plants than by non-infected plants, and feeding on citrus by ACP adults also induced the release of methyl salicylate. Methyl salicylate was attractive to ACP, while methyl anthranilate was not.44 The volatile profiles of the young leaves of six Rutaceae species were analysed in relation to the attractiveness of these species to ACP, which varied from highest to lowest as shown by the infested number of ACPs on them: Bergera koenigii (L.) (curry leaf tree), M. paniculata (L.) Jack (orange jasmine), C. macrophylla Wester, C. sinensis (L.) Osbeck ‘Valencia’, C. jambhiri Lush. (‘Rough’ lemon) and P. trifoliata (L.) (trifoliate orange).22 The results suggested a subset of likely candidate chemicals for evaluation in behavioural assays. For example, high concentrations of sabinene and 𝛽-phellandrene were found in attractive genotypes of C. sinensis (L.) Osbeck ‘Valencia’ and B. koenigii (L.) respectively, whereas large amounts of limonene were found in less attractive genotypes of C. jambhiri Lush. (‘Rough’ lemon) and C. macrophylla Wester.
5 WORK WITH OTHER INSECTS MAY PROVIDE CLUES FOR ACP REPELLENT RESEARCH DMDS has been reported as being repellent to other insects. The non-lethal repellent action of DMDS against adult mirid bug, Apolygus lucorum (a major pest of cotton, fruit trees and many other crops), was demonstrated under laboratory and field conditions.46 DMDS at a certain range of doses showed a significant repellent effect on potato psyllid, Bactericera cockerelli (Sulc), and it remained repellent during the whole 10 day longevity residual trial.47 𝛼-Pinene has repellent and toxic effects on the grain-storage insects Sitophilus zeamais, Rhyzopetha dominica and Tribolium castaneum.48 𝛽-Pinene has a repellent effect on grain moth Sitotroga cereallela.49 The response of Cryptomeria bark borer to the essential oil of Japanese cedar (Cryptomeria japonica D. Don) and its components was studied, and high repellent activity to Cryptomeria bark borer was shown by 𝛼-terpineol, nerolidol, 𝛿-cadinene and 𝛽-eudesmol of the oil.50 The sesquiterpene (E)-𝛽-farnesene was repellent to the pea aphid, Acyrthosiphon pisum (Harr), and the grain aphid, Sitobion avenae F.51 The feeding and egg laying of the carrot psyllid, Trioza apicalis, were reduced by application of fresh spruce and pine sawdust along the seedling rows in carrot fields.52 Recent research on the tritrophic system of pear trees, psyllid herbivores and anthocorid predators has indicated that the insects are highly attracted to methyl salicylate, possibly because infested pear trees are characterised by the odour of the chemical.53 Not coincidentally, feeding on citrus by ACP adults also induced release of methyl salicylate.44 These results suggest that methyl salicylate could be used practically as an attractant for psyllids. Pest Manag Sci (2014)
6 IS THE PUSH–PULL STRATEGY APPLICABLE IN CITRUS PSYLLID CONTROL? Effective control of ACP is an important component in a successful HLB management programme.25 In this regard, the push–pull strategy should be explored experimentally, as the method has potential to offer not only efficient control of ACP populations but also less significant adverse effects on the environment. Signs have been accumulating that the strategy works practically. As already mentioned, habitat diversification by intercropping citrus with guava showed a good effect on repelling ACP, although the efficacy varied in different studies. The currently known chemicals from limited studies on repellent plants have yet to be put into use in the field, but they can be chemically modified to be more effective. In addition, more effective chemicals may also be discovered if more repellent plants are investigated. Chemicals in volatiles of ACP host plants are similarly promising if used as attractants after chemical modification or used in combination after formulating the best of them together. In addition, modern genetics may be a pathway to modifying the host plants so that they will no longer be attractive to ACP. Before a practical pull–push method can be developed, a deeper knowledge of the behaviour of ACP and the interactions of this insect with its host plants is needed.
ACKNOWLEDGEMENT This work was supported by the International Science and Technology Cooperation Programme of China (Grant No. 2012DFA30610) and the Science and Technology Planning Project of Guangdong Province (Grant No. 2012A020200016).
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