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Potential for using semiochemicals to manage whiteflies (Hemiptera: Aleyrodidae) in agricultural fields

利用信息化学物在田间控制粉虱(半翅目:粉虱科)的潜力



全 文 :植物保护学报 Journal of Plant Protection, 2016, 43(1): 5 - 17 DOI: 10􀆰 13802 / j. cnki. zwbhxb. 2016􀆰 01􀆰 002
基金项目:国家自然科学基金 (31272089), 国家“973”计划(2013CB127600)
∗通讯作者(Author for correspondence), E⁃mail: txliu@ nwsuaf. edu. cn
收稿日期: 2015 - 10 - 28
Potential for using semiochemicals to manage
whiteflies (Hemiptera: Aleyrodidae)
in agricultural fields
Darshanee Hewa Lunuwilage Chamila1,2   Liu Tong⁃Xian1∗
(1. Key Laboratory of Crop Pest Management on the Northwest Loess Plateau of Ministry of Agriculture;
State Key Laboratory for Crop Stress Biology for Arid Areas, Northwest A & F University, Yangling 712100,
Shaanxi Province, China; 2. Department of Export Agriculture, Kandy 1095, Sri Lanka)
Abstract: Whiteflies cause serious crop losses in a broad range of agricultural crops worldwide. In
response to this scenario, considerable amount of researches have been directed towards finding cost
effective, environmental friendly solution to manage whiteflies and also to control the virus transmission.
In the Integrated Pest Management (IPM) approach, use of semiochemical is one of the best solutions to
minimize the over use of chemical pesticide. The evidences relate on semiochemical attractant or repellent
identification for whitefly has not yet been proven. However, semiochemical attractant could be a possible
tool for whitefly monitoring and management in crop fields since much of the behavioral responses of
whiteflies are associated with semichemicals. Therefore, the main objective of this review article is to
discuss the potential approaches to develop novel whitefly manipulation technique in the future while
addressing environmentally friendly crop management practices with special reference to semiochemical
attractant.
Key words: whiteflies; semiochemicals; herbivore induced plant volatiles
利用信息化学物在田间控制粉虱(半翅目:粉虱科)的潜力
Darshanee Hewa Lunuwilage Chamila1,2   刘同先1∗
(1. 西北农林科技大学, 旱区作物逆境生物学国家重点实验室, 农业部西北黄土高原作物有害生物综合治理
重点实验室, 陕西 杨凌 712100; 2. Department of Export Agriculture, Kandy 1095, Sri Lanka)
摘要: 粉虱取食为害以及传播植物病毒给全球作物生产带来重大危害。 寻求高效、经济、环境友好
型的防控方法成为当务之急。 在害虫综合防治中化学信息素的使用可有效减少化学农药的用量,
然而目前并没有实际可用的防治粉虱的化学信息素类产品。 鉴于挥发性化学信息素在粉虱行为反
应中的重要作用,以此开发的化学引诱剂将在粉虱监测和防治中起到重要作用。 本文主要综述了
植物 -粉虱 -天敌之间的信息化合物研究进展,重点关注粉虱相关的挥发性信息化合物,及基于此
类化合物开发新型防治技术和作物栽培管理策略。
关键词: 粉虱; 化学信息素; 植物挥发物
1 Introduction
    Whiteflies (Hemiptera: Aleyrodidae) are consid⁃
ered to be one of the most detrimental pests in the
world and they cause substantial annual crop losses,
either by their direct feeding behavior or ability of
transmitting plant viruses (Cameron et al. ,2013;Su et
al. ,2013). Among all the whitefly species, Bemisia
tabaci (Gennadius), Trialeurodes vaporariorum (West⁃
wood) and Trialeurodes ricini (Misra) are the promi⁃
nent whitefly species which are responsible for virus
transmission especially genus Begomovirus, Crinivirus,
Closterovirus, Ipomovirus and Torradovirus ( Jones,
2003; Liu et al. , 2012; Verbeek et al. , 2013;
Ovcˇarenko et al. ,2014a; Rosen et al. ,2015 ). The
whiteflies are polyphagous insects with piercing and
sucking mouthparts ( Inbar & Gerling,2008;Basit et
al. ,2013;Huang et al. ,2014) and responsible for cre⁃
ating serious crop damages in a wide range of field
crops and more than 600 different plants species have
been observed as a host for B. tabaci (Oliveira et al. ,
2001). Therefore, during the off⁃seasons, insects can
easily survive on alternative host plants and multiple
damages can arise in the following season with a high
level of pest abundance. Due to their selecting behav⁃
ior for host plants as a generalist herbivore, damage se⁃
verity can be varied on different crops such as castor,
pepper, eggplants, potato, pumpkin, cotton, green
beans, tomato, melon, cucumber, sweet potato and al⁃
so greenhouse crops and ornamental plants (Liu et al. ,
2012;Huang et al. ,2014;Prabhaker et al. ,2014).
In case of virus infections remarkable yield losses
have been recorded in worldwide agricultural lands
(Oriani et al. ,2011). The yield reduction of tomato
cultivations in the most whitefly affected areas of the
world are around 100% ( Morales & Jones, 2004 )
whilst, at the sever stage of B. tabaci damage, approx⁃
imately 90% of yield reduction is recorded in suscepti⁃
ble cotton cultivations in North India ( Singh et al. ,
2013). Furthermore, whitefly B. tabaci has rapidly
spread in most part of the China and cause severe crop
losses of tomato productions in awfully infested areas in
the country (Hu et al. ,2011;Guo et al. ,2012).
The most curious aspect of this insect’ s behavior
is the unexpected adaptation to different environmental
conditions due to their wide host range, high reproduc⁃
tive potential and sudden resistance development ability
(Mansaray & Sundufu,2009). Behavioral responses of
the whiteflies can also be altered by host plants and
their nutritional level. A high nutritional value in
plants helps the rapid development of B. tabaci be⁃
cause both offspring and adults are able to feed on the
host plants. This can create a different attraction be⁃
tween plant species. As an example, B. tabaci has a
preference to colonies the poinsettia plants rather than
the tomato plants ( Jing et al. ,2003). In addition,
even given the same temperature and relative humidity,
total life cycle development time can also be changed
with plant variety. In comparison with soybean Glycine
max plants, whiteflies show greater performance on
garden bean Phaseolus vulgaris plants ( Mansaray &
Sundufu,2009). Nitrogen concentration in cherry to⁃
mato plants impact on the development time of eggs
and nymphs of greenhouse whitefly T. vaporariorum
and nitrogen levels are positively correlated with the fe⁃
cundity rate of the whiteflies ( Park et al. , 2009 ).
Feeding and ovipositional performance of T. ricini is
also not similar on castor, eggplant, cotton and green
bean plants (Huang et al. ,2014). It implies that the
preference of whiteflies for different plant species is not
similar because of the extraordinary disparity of plant’s
physiological, morphological and chemical characteris⁃
tics. Among all these characters, whiteflies have high
capacity to select their host plants using plant olfaction
cues and herbivore can easily detect the most suitable
host plant from a distance ( Jing et al. ,2003). The
odour blends may act as an instantaneous and reliable
indicator of host suitability to herbivore pests (Zhang et
al. , 2009 ). Subsequently, insects also emit semio⁃
chemicals by themselves or by inducing plants to intra⁃
specific or inter⁃specific attraction. The emitted com⁃
pound can be a pheromone, kairomone, allomone or
synomone (Loughrin et al. ,1995). Survival ability of
the insect pests depends on their capacity to identify
the specific volatile chemicals in the environment since
odour cues are used in finding their mates, locating
feeding areas, aggregating regions as a group, protec⁃
ting from natural enemies and finding the oviposition
6 植  物  保  护  学  报 43 卷
sites (de Bruyne & Baker,2008). The herbivore at⁃
tractive semiochemicals facilitate to monitor the size of
their population throughout the year (Weinzierl et al. ,
2005). Although whitefly damage is a remarkable
problem around the world, an effective semiochemical
compound being used in the field against whiteflies has
not yet been found to practice in the field conditions.
In⁃depth knowledge of whitefly population in agri⁃
cultural fields and their interaction with conspecifics,
host plants, competitors and also natural enemies is es⁃
sential to recognize a successful management package.
Thus, semiochemical attractant could be a useful tool
for whitefly monitoring and management. The main ob⁃
jective of this review article is to discuss the current
whitefly management strategies and observe the poten⁃
tial possibilities to develop novel management approa⁃
ches in the future with performing agro⁃ecosystem sus⁃
tainability.
2 Current whitefly management
2􀆰 1 Chemical control
The conventional farmers in both developed and
developing countries use high amounts of agrochemicals
to manage whiteflies in agricultural fields. Readily
availability, quick results and ease of use with mini⁃
mum labor costs are the main reasons for high usage of
agrochemicals. However, throughout the world, white⁃
fly management remains major challenge using chemi⁃
cal pesticides due to their ability to development of
sudden resistance and the feeding behavior underside
of the leaf surfaces (Erdogan et al. ,2012;Rao et al. ,
2012;Horowitz & Ishaaya. , 2014; McKenzie et al. ,
2014; Ovcˇarenko et al. ,2014b), and further, it cre⁃
ates many environmental hazards and the most attention
are driven back with the natural enemies of whiteflies.
Chemical pesticides imidacloprid and buprofezin nega⁃
tively affect on the performance of whitefly parasitoid
Eretmocerus mundus Mercet ( Sohrabi et al. , 2013 ).
Prior to apply insecticides in agriculture fields, identi⁃
fication of peak flight duration of whiteflies is one of the
major tactics to diminish the unnecessary application of
insecticide. Additionally, the effective life stage of tar⁃
get insect and time interval between two applications of
insecticides should also be considered. In chemical
treatment practices, it is also vital to consider about the
impact on environment and compatibility with natural
enemies. Hence, to reduce the crucial aspects of the
chemical pesticides utilization, alternative whitefly
management measure based on semiochemical attract⁃
ant should be implemented to avoid redundant utiliza⁃
tion of chemical pesticides in agricultural fields.
2􀆰 2 Environmental management and plant semio⁃
chemical production
The environmental factors and also host plant
characteristics have diverse effect on the whitefly popu⁃
lation genetic structure and biological features
(Ghafoor et al. ,2011;Curnutte et al. ,2014;Huang et
al. ,2014;Ovcˇarenko et al. ,2014a) and therefore, en⁃
vironmental changes may have tremendous influence to
diminish whitefly damage in agricultural fields. In con⁃
trast to behavioral changes of insects, plants also pro⁃
duce diverse volatile organic compounds (VOCs) un⁃
der the various environmental conditions and these vol⁃
atiles change the attraction of herbivore insects and
their natural enemies as well (Shiojiri et al. ,2006;Ho⁃
lopainen & Gershenzon,2010; Zhang et al. ,2010).
The light intensity of the surroundings is one of the ma⁃
jor aspects to change the plant volatile emission (Gou⁃
inguene & Turlings,2002; Zhang et al. , 2010 ) and
these volatile compounds possibly advantageous for
avoiding crop plants colonization by pests. Consequent⁃
ly, host plants keep under favorable volatile emission
light condition especially in the greenhouse without
harming to the growth of plants may be worth to dimin⁃
ish whitefly damaged.
Sustainable management of agro⁃ecosystems is es⁃
sential to obtain well⁃functioning tropic interactions
since modern homogeneous farming practices signifi⁃
cantly reduce the vegetational diversity where agricul⁃
tural lands are not favor to natural enemy activities
(Tscharnke et al. ,2005). Further, uniform homoge⁃
neous cultivation influence the severe pest pressure
with optimum food resources for herbivore pests (Lan⁃
dis et al. ,2000). However, herbivore pest manage⁃
ment is better than the eradication because pest eradi⁃
cation is harmful for their natural enemies as well as
agro⁃ecosystem stability. Therefore, biodiversity man⁃
agement based on the semiochemical properties of
71 期 Darshanee Hewa Lunuwilage Chamila, et al. : Potential for using semiochemicals to manage whiteflies
plants is a sound endeavor for well⁃functioning tritropic
interactions between plants, herbivore and their natural
enemies and it might be the best solution to manipulate
whitefly population in agricultural fields. To enhance
the benefits of semiochemical activities in diversified
agricultural fields, different techniques are currently
performed.
In trap cropping method, crop selection mainly
depends on the host plant preference of target herbivore
and then, cultivate them together with main crop to
suppress the abundance of the pests’ population on
major crop ( Banks & Ekbom, 1999 ). In designing
successful trap cropping system, interaction between
plant species and the target herbivore should be consid⁃
ered as a foremost important factor. The tomato Lycop⁃
ersicon esculentum plants show remarkable reduction of
Yellow leaf curl virus when it intercrops with cucumber
Cucumis sativus plants (Al⁃Musa,1982) whilst cucum⁃
ber plants have higher capability to attract B. tabaci
compared with tomato and egg plants Solanum melon⁃
gena (Ding et al. ,2015). A further study observed
the cucumber plants as a trap crop around the poinset⁃
tia cultivation to reduce the damage by B. argentifolii
(Lee et al. ,2011). Additionally, B. tabaci damage is
declined on the cotton plants when it grows with the
sunflower as a trap crop ( Zheng et al. ,2013). Egg
plants also have significant semiochemical properties to
attract T. vaporariorum as a trap crop near to the sweet
pepper crop fields (Moreau & Isman,2010).
The push⁃pull technique uses semiochemicals of
intercropping plants in the fields to repel major pest
from crop plants and then, attracted by surrounding
trap crops. The whitefly B. tabaci population signifi⁃
cantly decline on the egg plants when it intercrops with
marigold plants and cultivate maize as a border crop
(Sujayanand et al. ,2015). The essential oils of lob⁃
ster flower plants Plectranthus neochilus has repellent
ability against B. tabaci due to its’ (E)⁃caryophyllene,
monoterpenes α⁃pinene and α⁃thujene content (Baldin
et al. ,2013) and it has been suggested that tomato
plants intercrop with P. neochilus help to repel white⁃
flies from main crop.
The odour masking ability of the plants plays a
pivotal role to obstruct the herbivore pest performance
in agricultural lands. The coriander plants facilitate to
suppress the B. tabaci pest pressure on main crop to⁃
mato (Togni et al. ,2010). Especially, in the mixed
cropping systems, as a generalist herbivore whitefly B.
tabaci is unable to make the direct decision to select
one plant and show lots of movements from plant to
plant possibly the result of odour masking ability of
non⁃crop plants ( Bernays, 1999; Tosh & Brogan,
2015). In the plant odour mix environment, not only
B. tabaci but T. vaporariorum also shows remarkable
behavioral differences due to confusion effect by plant
odours (Tosh & Brogan,2015).
Moreover, the conservation biodiversity manage⁃
ment augments the activity of natural enemies while
suppressing the damage of whiteflies ( Naranjo,
2001). Habitat conservation and provide more food
sources for natural enemies are outstanding attempts to
enhance the population density of them in agricultural
fields (Landis et al. ,2000). The population density of
T. vaporariorum on common bean Phaseolus vulgaris
cultivations can be diminished by growing non⁃crop
plants around the fields since vegetational environment
influences the activity of parasitoids Amitus fuscipennis
MacGown & Nebeker (Hernandez et al. ,2013) where⁃
as in the tomato cultivations with weeds reduce the
damage of B. tabaci and augment the activity of natural
enemies ( Bezerra et al. , 2004 ). These evidences
prove that diversified agro⁃ecosystem is unfavourable
for herbivore, because they may be difficult to find the
food sources in diversified agro⁃ecosystems with com⁃
parison to monoculture crop fields. However, whiteflies
are generalist herbivore and they can easily survive in
diversified fields. In diversified fields, generalist her⁃
bivore is also manipulated below economic threshold
level, due to significant expansion of natural enemy
population. Nonetheless, biodiversity management is
difficult to consider as an easy technique since both
negative and positive impacts mainly depend on funda⁃
mental knowledge and decision making ability of the
farmers when designing crop diversification systems.
Notwithstanding, genetic changes of whitefly B.
tabaci can be rapidly occurred to the adaptation for new
environment (Chu et al. ,2014) and as an example B.
tabaci biotype B out⁃compete with indigenous whitefly
8 植  物  保  护  学  报 43 卷
species and replace them (Liu et al. ,2010). These
evidences prove that whitefly management strategies
should be developed on the observable ways to accom⁃
plish the target in the diversified agro⁃ecosystems.
2􀆰 3 Responses of natural enemies to semiochemicals
The management of whiteflies using biological
control agents is a widespread technique in modern ag⁃
ricultural systems that achieve the most promising re⁃
sults. The parasitoids Encarsia formosa Gahan and Er⁃
etmocerus mundus Mercet are the most important natu⁃
ral enemies to control whitefly B. tabaci and T. vapo⁃
rariorum and T. ricini in agricultural lands ( Speyer,
1927;Guerrieri,1997;Pickett et al. ,2013). Simulta⁃
neously, predatory mirid Macrolophus pygmaeus
(Rambur) has long been used as a biological control
agent to control the whitefly T. vaporariorum (Bresch
et al. ,2014). Natural enemies also use olfaction cues
which is emitted by whitefly as well as host plants to
find their pray ( Halitschke et al. , 2008; Kurra &
Pathipati,2015; Liu et al. ,2015). In the poinsettia
cultivations, the whitefly B. argentifolii Bellows & Per⁃
ring ( = B. tabaci biotype B) damage is low when use
the predator Delphastus catalinae Horn on poinsettia
and cultivate cucumber as a trap crop around the field
(Lee et al. ,2011). The natural enemy activities will
enhance with the presence of more pests due to the
availability of more food sources for them.
Further, to obtain significant results from biologi⁃
cal control agents especially parasitoids and predators,
they can be provided artificial semiochemical source to
prolong the attraction of them. It might possibly a good
influence to hinder the growth of whitefly population.
In a recent study, Roopa et al. (2014) has identified
three species of bacteria from honeydew of B. tabaci
which might be a good source to induce the attraction
of natural enemies and in some circumstances, honey⁃
dew also responds as a kairomone for host searching
behavior of herbivore pests whereas the aphid honey⁃
dew remarkably attracts their parasitoid Aphidius nig⁃
ripes Ashmead (Bouchard & Cloutier,1984).
However, specificity of natural enemy, their fa⁃
vorable environmental factors, application time should
be considered as important features which impact of the
efficacy of biological control strategies on whitefly man⁃
agement (Speyer,1927). The most obvious factor as⁃
sociated with biological control is the reduction of un⁃
necessary usages of chemical pesticides with providing
farmer friendly environment. The highest greenhouse
crop production in the world is recorded from China
and dealing with biological control approaches in the
greenhouse is therefore more precise environmental
friendly and cost effective technique ( Yang et al. ,
2014). In contrast, the most problematic impact of the
biological control is not easy to manage at the sudden
pest out breaks and farmers should have the knowledge
about biological and ecological parameters of the intro⁃
duced natural enemy. Moreover, to augmentation the
population density in the field, frequent introduction of
the natural enemy is essential. Therefore, the pest
management using biological control is much more in⁃
tensive than the other control approaches.
2􀆰 4 Herbivore induced plant volatiles
A plant usually produces a mixture of volatile
compounds at the normal condition and the composition
may differ in regards to the situation of plant such as
herbivore damaged, mechanical damaged or undam⁃
aged. The plants are known to produce chemical com⁃
pounds after feeding or egg deposition by an herbivore
call herbivore induce plant volatiles ( HIPVs). The
HIPVs may be beneficial for plants as well as for carni⁃
vore insects and in special circumstances it may be a
forging cue to the herbivore (Dicke et al. ,2009;Dicke
& Baldwin,2010;Gish et al. ,2015). Miresmailli et
al. (2010) reported that the level of the two⁃spotted
spider mite Thetranychus urticiae Koch infestation and
their feeding duration on the plants affect to emission of
qualitatively and quantitatively different plant volatiles.
Additionally, the most of the studies indicated that
HIPVs attract natural enemies of herbivore in indirect
defense of plants ( Kurra & Pathipati, 2015 ). The
greenhouse whitefly T. vaporariorum infested bean
plants emit the volatiles that attract natural enemy E.
formosa (Birkett et al. ,2003). But few of the articles
mentioned that HIPVs attract other herbivores or their
conspecifics to infested plants ( Dicke & van Loon,
2000;Dicke & Baldwin,2010 ). As an example for
multiple herbivore attraction by plants is B. tabaci in⁃
fested plants influence the attraction of the spider mite
91 期 Darshanee Hewa Lunuwilage Chamila, et al. : Potential for using semiochemicals to manage whiteflies
T. urticea, and suppress the attraction of predatory
mites Phytoseiulus persimilis Evans in lima bean plants
(Zhang et al. ,2009).
Semiochemicals of host plants or whiteflies might
play an important role in attracting their conspecifics
from the distant places. In regards to the use of semio⁃
chemicals to implement a control strategy, it is impor⁃
tant to identify which volatile compound is recognized
by whiteflies at an olfactory level and what is the mini⁃
mum dose eliciting a remarkably large number of be⁃
havioral attraction of the target insect (Corrado et al. ,
2007). Salicilic acid and methyl jasmonate mediated
signaling pathway in the plants plays a pivotal role
against phloem feeding grain aphid, Sitobion avenae
(Fab. ) ( Cao et al. ,2014 ). This evidence proved
that salicylic acid and also methyl jasmonatehave possi⁃
bility to affect on whitefly developments since they are
also the phloem feeding insects. Shoot jasmonic acid in
Chinese broccoli, Brassica oleracea var. alboglabra,
directly affect on whitefly, B. tabaci development and
their survivorship (Li et al. ,2013). The tomato plants
which were infested by aphids Myzus persicae ( Sulz⁃
er), produce chemical compounds that repel the white⁃
fly, B. tabaci (Tan et al. ,2014) and attract natural
enemies of both whiteflies and aphids ( Tan & Liu,
2014). Additionally, the spiraling whitefly Aleurodicus
dispersus Russell response to the volatiles release from
the plant Pterocarpus indicus Willd. ( Zheng et al. ,
2014). Female B. tabaci is highly attractive to the
non⁃infested chilli ( Capsicum annum cv. Kulai )
plants compared with previously whitefly infested chilli
plants (Saad et al. ,2013). On the basis of these evi⁃
dences, recent plant genetic engineering attentions
have been mainly converted to produce transgenic
plants with HIPVs attract natural enemies or both to
manage herbivore pest population in agricultural fields.
2􀆰 5 Genetic engineering usages to induce plants
semiochemical volatiles
The pest management technologies get on novel
manifestation with the biotechnological usages in the
crop protection while reducing the chemical pesticide
applications. This approach can be utilized with other
alternative methods, thereby providing an ecologically
sound pest control strategy without damaging to agro⁃e⁃
cosystem stability. Genetically modified ( GM) crops
with high yield and pest resistant varieties have been
developed by using high technology ( Tscharntke et
al. ,2005 ). Among them, several transgenic plants
with volatile organic compounds ( VOCs) support to
natural enemy attraction and repel the herbivore.
HIPVs especially terpenoids are the well⁃known HIPVs
play an important role to attract predators or parasitoids
of herbivore pests ( Kappers et al. , 2005; Mumm et
al. ,2008 ). Genetic engineering technology can be
used to generate these beneficial volatile compounds at
the normal condition of transgenic plants as an advanta⁃
geous pest management strategy. A team of researchers
observed that the possibility of transgenic maize plants
to produce defense signals using VOCs to attract para⁃
sitoid, Cotesia marginiventris (Cresson), of maize her⁃
bivores (Schnee et al. ,2006). Besides, some plants
produce VOCs to attract herbivore pest as well as their
natural enemies. The transgenic Nicotiana attenuate
plants emit the volatiles to attract both tobacco horn⁃
worm, Manduca sexta (Linnaeus), and their predatory
bug, Geocoris punctipes ( Say), and it facilitates to
suppress the population density of herbivore on tobacco
plants ( Halitschke et al. , 2008 ). Transgenic rice
plants also release VOCs to attract egg parasitoids to
control herbivore pests ( Cheng et al. , 2007 ) and
S⁃linalool and (E)⁃β⁃caryophyllene production induce
the attract of natural enemies while repel rice brown pl⁃
anthopper, Nilaparvata lugens (Stål), and then, only
( E)⁃β⁃caryophyllene production attract both natural
enemies and herbivore (Xiao et al. ,2012).
These evidences proved that volatile emissions
from transgenic plants are advantageous to manage the
herbivore pest pressure in the fields. So far there is no
any evidence about the transgenic plant produce VOCs
to manipulate whitefly population in the fields. Howev⁃
er, the whitefly B. tabaci resistant water melon is cul⁃
tivated in the field to suppress the pest pressure (Sim⁃
mons et al. ,2010) and the okra⁃cultivar “ IS⁃376 / 4 /
1⁃40 × RS⁃2013” appears to have genetic traits resist⁃
ance for the B. tabaci damage ( Nogia & Meghwal,
2014) while interestingly, resistant genotype of cowpea
for B. tabaci has also been identified to tackle the
whiteflies damage ( Cruz et al. ,2014). In contrast,
01 植  物  保  护  学  报 43 卷
Singh et al. (2013) observed the susceptibility of Bt
cotton for the B. tabaci transmitted Geminivirus and
this study implies that whiteflies might gradually devel⁃
op resistance for the Bt cotton.
Even with the more advantages from transgenic
plants, various potential negative impacts for target
herbivore as well as non⁃target organisms such as polli⁃
nators and natural enemies is still expected. Moreover,
out⁃crossing with traditional varieties may be a risk to
generate unexpected plant genotypes. The other curi⁃
ous aspect of the GM plants is pest resistance develop⁃
ment. Continues releasing of HIPVs from transgenic
plants may negatively affect on the plant physiological
characters ( Gish et al. ,2015). Hence, the experi⁃
ments relate with transgenic plants for HIPVs are still
performed under experimental condition and utilization
of commercialized large scale fields is questionable yet
(Kaplan & Lewis,2015).
2􀆰 6 Semiochemical traps in agricultural fields
Monitoring, mass trapping, mating disruption and
lure⁃kill methods are prominent techniques of using
semiochemicals in crop fields to control herbivore
pests. However, several factors such as trap color,
trap type, trap density in the field and trap establish⁃
ment height are important factors to be considered when
establishing semiochemical traps to gain optimum effi⁃
cacy. Trap color may influence the attraction of benefi⁃
cial insects (Knight,2010). Therefore, when desig⁃
ning pest management systems using pheromones, traps
color is one of the important characteristics. Clare et
al. (2000) confirmed that white, yellow and blue color
traps attract large amount of honey bees Apis mellifera
Linnaeus compared to red and green sticky traps. Fur⁃
ther, it has been suggested that trap color does not im⁃
pact on the target insects Cydia pomonella (Linnaeus)
and Epiphyas postvittana (Walker) . However, in con⁃
trast, the trap color is an essential factor for whitefly
attraction (Chu et al. ,2004).
The spiraling whitefly, Aleurodicus dispersus Rus⁃
sell, attracts to the LED light trap ( Zheng et al. ,
2014) and B. tabaci also shows the positive phototac⁃
tic behavior with presence of the light ( Summers,
1997). However, their phototactic behavior depends
on the age whereas young B. tabaci up to five⁃days⁃old
is more attracted to the target host but from six⁃days⁃
old to onwards whiteflies have high phototactic behavior
towards to the target illumination ( Blackmer et al. ,
1995). It might be a positive point for managing white⁃
flies damage since young whiteflies have low capacity to
transmit the viruses rather than the older insects (Czos⁃
nek & Ghanim,2012). But, pre⁃ovipositional period
of whiteflies last approximately one day and their ovipo⁃
sition takes place from the second day ( Enkegaard,
1993). Therefore, if we can control the whitefly adults
at younger stage before they reach to older age, it
would be beneficial to future crop cultivations world⁃
wide. Moreover, whiteflies B. tabaci and T. vaporari⁃
orum exhibit positive phototactic orientation to green
LED lights and among them viruliferous B. tabaci has
high attractiveness to green LED lights ( Jahan et al. ,
2014). The UV⁃A radiations also have effect on white⁃
fly biological features ( Dáder et al. , 2014 ). Apart
from these evidences, Chu & Henneberry (1998) ob⁃
served the possibility to attract whitefly by special kind
of trap name CC trap containing yellow color base.
These traps have been confirmed its suitability for
catching whiteflies compared with yellow color sticky
traps on cost⁃effective and ecological basis. Then, in
2003 two research groups also again proved the adverse
effect of yellow sticky traps for whitefly control in
greenhouses due to attraction of large amount of Eret⁃
mocerus mundus Mercet, Er. eremicus Rose & Zolner⁃
owich, E. formosa (Chu et al. 2003;Nombela et al. ,
2003). Afterward, considering the response of whitefly
attraction to trap color and the light traps, Chu and his
colleagues suggested to use lime green LED equipped
with yellow sticky traps as a potential trap design for
whitefly attraction in agricultural fields due to their
phototactic flight behavior.
Appropriate trap type should also be considered to
obtain significant reduction of target pest population in
the fields. Among the different trap types, sticky traps
are suitable to capture high density of lepidopteron in⁃
sect pest ( Trematerra,1997) due to their soft, scale
wings help easily stick on the sticky surface of the semi⁃
ochemical traps. The codling moth, C. pomonella, in
apple orchard can be easily captured by deploying clear
delta traps baited with pheromones (Knight,2010).
111 期 Darshanee Hewa Lunuwilage Chamila, et al. : Potential for using semiochemicals to manage whiteflies
The number of traps in the fields is another note⁃
worthy aspect to deem when establishing semiochemical
traps in the field. For instance, most suitable trap den⁃
sity to control potato tuber moth Phthorimaea operculel⁃
la ( Zeller) is 20 pheromone traps per hectare with
comparison to 10 traps / hm2 and 40 traps / hm2(Larrañn
et al. ,2009) and appropriate amount of trap density in
the field perform profit maximization and efficacy of tar⁃
get pest control. In pest management strategies using
pheromone traps, trap establishment height augment
the activity of male insect against pheromone odour
plume and. in vineyards the most suitable pheromone
dispenser establishment height is between 0􀆰 1 m to 1􀆰 4
m from ground level to control vine moth Lobesia botra⁃
na (Denis & Schiffermuller) (Sauer & Karg,1998)
On the basis of these researches, designing traps
according to the behavioral pattern of whiteflies may al⁃
so be a good option for enhancing the amount of white⁃
flies catches into the semiochemical traps.
3 Future perspectives to use semio⁃
chemicals to manage whiteflies
    The comprehensive management strategies for pro⁃
tecting crops from whiteflies are constantly being re⁃
quired. Sustainable agriculture is a modern theme in
the worldwide agricultural systems (Pretty,2007;Man⁃
saray & Sundufu,2009) and in response to this prob⁃
lem, a considerable amount of research has been di⁃
rected towards finding cost⁃effective solutions to man⁃
age whiteflies and also to control the virus transmis⁃
sion. The global agriculture is turning to environmen⁃
tally friendly crop management practices with special
reference to pest control strategies known as IPM (Koul
& Walia,2009). IPM techniques greatly support to har⁃
monize coordination of farm management practices using
farmer’s decision making ability and their resources.
The chemical diversity in nature is fascinating.
Plants, herbivores and carnivores produce different
types of chemical compounds whereas certain chemical
compounds are connected through their food webs to
create tropic interactions. These chemical compounds
are considered as semiochemicals and they serve a spe⁃
cific function or several functions in nature as they car⁃
ry out messages for insect pests over considerable dis⁃
tances. At the beginning, only some researches indica⁃
ted that the greenhouse whitefly T. vaporariorum re⁃
lease specific volatiles to attract their conspecifics (Yin
& Maschwitz,1983;Birkett et al. ,2003). Afterward,
there is no any evidence regarding the volatiles pro⁃
duced by whiteflies. Though, the tropic interactions
are mainly related with olfaction cues of plant volatiles
(Ahmad et al. ,2004;Bleeker et al. ,2009). Hence,
plant semiochemicals can be used as one of the most
advantageous component in IPM to manipulate the in⁃
sect behavior and monitor the size of insect population
throughout the year (Heuskin et al. ,2011). Current
whitefly monitoring practices in farmer fields are per⁃
formed with yellow sticky traps due to their ability to
attract whiteflies by the yellow color (Pinto⁃Zevallos &
Vãnninen,2013). Insects exploit olfactory cues to find
their host plant and then, visual cues are used to land
on the plants (Bleeker et al. ,2011). Hence, yellow
sticky traps might not be a useful tool to attract the
whiteflies from distant places in the fields without pre⁃
cise semiochemical attractant. Fascinatingly, this hy⁃
pothesis is proved by Chen et al. (2015) since they
have observed the highest efficacy of yellow sticky traps
with sex pheromone to attract diamondback moth Plute⁃
lla xylostella (Linnaeus) and Liriomyza spp. In recent
years, there have been extensive studies on the plant
derived volatile chemical compounds and the interac⁃
tion between herbivores and their host plants. The wild
tomato plants produce curcumine, sesquiterpene and
zingiberene by leaf surfaces that are toxic to whiteflies
(Bleeker et al. ,2009) and terpenoid production of to⁃
mato plants change the response of whitefly attraction
(Bleeker et al. ,2011). Nevertheless, the experiments
relate on semiochemical attractant or repellence identi⁃
fication for whitefly is still in its infancy. Hence, to
gain optimum efficacy from semiochemical⁃based white⁃
fly management strategies in crop fields, it is necessary
to consider the behavioral response of whiteflies related
to the target semiochemicals. Additionally, appropriate
identification of chemical compound and its natural
concentration is imperative to produce semiochemicals
synthetically.
As an important advantage, semiochemical traps
do not require high maintenance capacity and no barri⁃
21 植  物  保  护  学  报 43 卷
er to other crop management practices especially har⁃
vesting. Hence, it is easy to practice without additional
labour cost and furthermore, the pheromone attractants
are species⁃specific (Hardie et al. ,1990), non⁃toxic,
less impact on non⁃target beneficial insects ( Clare et
al. ,2000), keep the pests population below economic
threshold level throughout the year and facilitate to de⁃
termine spatio⁃temporal distribution of the pest popula⁃
tion (Trematerra et al. ,2007). On the contrary, just
pheromone treatment is not critical strategy to manage
whitefly population in the agricultural fields since it
may attract only mature stages of target pests even in
special circumstance damage is occurred from both ma⁃
ture and immature life stages of the target pests. Cli⁃
matic parameters such as environmental temperature di⁃
rectly affect on the trap catches of target pest (Delisle,
1992) and it might alter with catch size in the different
climatic regions in the world. Extraordinarily, HIPVs
shows more problematic views like non⁃target herbivore
attraction, hinder the activity of natural enemies due to
unavailability of pray. Then, the composition of HIPVs
on transgenic plants may differ in stress environmental
condition and it negatively affects on the multitrophic
interactions of plants, herbivore and natural enemies
(Blande et al. ,2014; Gish et al. ,2015). Further⁃
more, dispersal ability of the natural enemies is also
important factor when designing HIPVs control strategy
since some natural enemies have low dispersal ability
compared with their pray (Tscharnke et al. ,2005;Ka⁃
plan & Lewis,2015). Therefore, achieving the target
by HIPVs in large scale fields might not be possible
due to their insignificant dispersal performance in the
middle part of the fields.
In assessing all the facts to control the whiteflies,
difficult to find trouble⁃free single approach, because it
is essential to assume possible hazardous of whitefly
manipulation strategies on herbivore suppression, natu⁃
ral enemy enhancing, reduction of secondary pest out
breaks, environmental risk and also cultivated crop
species. Therefore, development of environmentally
sound IPM package is appropriate while addressing all
the favorable techniques. Moreover, sustainable agri⁃
culture will enhance agro⁃ecosystem integrity and sus⁃
tainability, even though insecticides are also being
used in the IPM approaches. To optimize the outcome
from IPM, monitoring of the whitefly population is con⁃
sidered a moral option to detect the appropriate time
point to use insecticides. Ideally, synchronize usage of
semiochemical attractant in IPM practices is suitable to
gain an idea about population dynamics of whiteflies
whilst obtaining a clue about the abundance of natural
enemy population in the fields.
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711 期 Darshanee Hewa Lunuwilage Chamila, et al. : Potential for using semiochemicals to manage whiteflies