annals of life sciences 11 (2018) 9 27 annals of life...
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9 Saghir et al
Annals of Life Sciences 11 (2018) 9–27
Review Article
Historical trend and future possibilities of whitefly on cotton: A Review
Saghir Ahmad1, Muhammad Rafiq Shahid1*, Muhammad Farooq2 and Muhammad Shahid Iqbal2*
1Cotton Research Institute, Multan, Pakistan
2 Cotton Research Station, Faisalabad, Pakistan
Corresponding Authors: [email protected]
ABSTRACT
In the current scenario, whitefly has become a big threat on cotton. It sucks cell sap and is carrier of cotton leaf curl virus (CLCuV). Very useful
developments have been accomplished regarding biology, ecology, behavior, and population dynamics of whitefly. Pest management system
against whitefly research shifted from conventional pesticide regimes to insect growth regulators. Use of pyrithroids remained uneffective in
controlling population of Bemesia tabaci due to insecticide resistance and negative effects of pesticides on beneficial fauna and resulted in
secondary pest outbreak. IGR’s are less harmful for beneficial fauna but are more effective and economical. This review article covers various
aspects of whitefly including systematics, bio-ecology and sustainable management of whitefly, but main focus of review article is to discourage
conventional insecticides and to promote use of new chemistry insecticides and bio-control agents against cotton whitefly.
Taxanomy and nomenclature
Whitefly, earlier recognized as
Bemisia tabaci (biotype B) currently known
as Middle East-Asia Minor 1. This species
was reported for the first time in America
during mid-1980s and recognized as new B.
tabaci strain (Brown et al., 1995). It has
been also called as biotype-B of Bemisia
tabaci until 1994. It was labeled as a
separate species and named as Bemisia
argentifolii by Bellows et al. (1994).
Characterizing B biotype as B. argentifolii
in comparison with only indigenous
American strain (A biotype) was issue for
taxonomists (Bedford et al., 1994). Detailed
morphological characteristics were
examined by Rosell et al. (1997) as
mentioned by Bellows et al. (1994) for
identification of Bemisia argentifolii now B
biotype has been recognized as Bemisia
argentifolii. Phylogenetic membership of B.
tabaci were examined during 2005 and six
discrete 'races' were detected throughout the
world. However, (De Barro et al., 2005)
described it insufficient molecular and
biological data for separation of Bemesia
tabaci from Bemisia argentifolii. Research
was further conducted on mitochondrial
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10 Saghir et al
cytochrome oxidase 1 gene (mtCO1) level.
It indicates that Bemisis tabaci is a group of
11 genetic makeups composed of more than
34 morphologically distinguishing species
(Dinsdale et al., 2010; Boykin and De Barro,
2014). It was accepted by taxonomists
throughout the world.
Geographical distribution of whitefly
First time infestation of whitefly was noticed
on cotton in India during the 20th century
(Hussain and Trehan 1933; Cowland, 1934;
Hussain et al., 1936) and it became a serious
pest there during 1980’s (David and
Jesudasan, 1985). After its severity of
infestation and recognition as a vector of
virus (Borror et al. 1989) in Sudan it became
number one insectpest of cotton in Sudan
(Kirkpatrick, 1931). Between 1970-80
plentiful outbreaks was recorded on cotton
in Sudan, Turkey and Israel (Dittrich et al.,
1985, 1990; Gerling et al., 1980); then
widened its host range and outbreak
occurred on vegetable crops and cotton in
California (Russell, 1957). In 1989-90 its
epidemic invasion was recorded on cotton in
USA, Maxico, South America and Asia.
Taxonomically it was considered as vector
of cotton leaf crumple virus and was
identified as Bemesia tabaci (Dickson et al.,
1954). Thereafter, Bellows et al. (1994)
described a new species of whitefly known
as silver whitefly, B-biotype or Bemesia
argentifolii. Its outbreaks were recorded on
cotton in USA (Russell, 1957) Israel and
Turkey (Gerling et al., 1980). It was
observed as a carrier of new strain of cotton
leaf crumple virus for the first time in USA.
However the outbreak of new species of
Bemesia argentifoli was observed for the
first time from USA (Bellows et al., 1994)
its outbreaks were reported during 1988 to
onward in several cotton growing areas of
Asia. Same strain B (B. argentifollii) is
primarily a threat for cotton in Pakistan and
India and is vector of cotton leaf curl virus
(Gerling and Henneberry, 1998). Currently
it has been distributed throughout the world
except Antarctica (Martin et al. 2000).
Nature of damage of whitefly
Whitefly produces loss by reducing crop
yield and increases cost of cotton production
due to the insecticide applications for its
control (Vieira el at. 2011). Both nymphs
and adults of whitefly suck cell sap, reduce
plant vigour by disturbance in
photosynthesis due to development of sooty
mould fungus Capnodium sp. (Oliveira et al.
2001) and transmission of more than 100
viruses (belonging to group carlavirus,
closterovirus, geminivirus, luteovirus and
11 Saghir et al
potyvirus) which transfer diseases in plants
throughout the world (Jones, 2003) in
different crops (Morales and Anderson
2001), however in cotton it is carrier of
Cotton leaf curl virus that are persistent-
circulative in the whitefly bodies (Cohen,
1986).
Whiteflies also induce loss by honeydew
excretion that lead to spinning problem
through stickiness and deteriorate quality of
fiber (Attique, et al., 2003). However,
economic loss may be variable depending
the severity of infestation, stage of the crop,
availability of host plants and disease
carrying specimens as well as the climatic
conditions favoring whitefly and disease
(Prabhaker et al., 2005). In Brazil economic
loss due to whitefly were reported 30-100 %
depending upon the severity of disease
(Vilarinho de Oliveira, 1998) because
whitefly vector was responsible for loss of
1.0 M ha of cotton in the country due to
Cotton leaf curl virus attack (Mansoor et al.,
1993).
Host range of whitefly
Despite of cotton it invade over 500 plant
species from Africa, America, Asia,
Australia, Europe, Pacific Islands and
Russia. Due to polyphagous nature it causes
severe damage to cotton, mungbean,
soyabean, okra, brinjal and other economic
crops (Jose and Usha, 2003; Nauen and
Denholm 2005). But it is thought of the
researchers that international trade in
poinsettia and gerbera is significant source
of whitefly dispersal throughout the world
(Cuthbertson, 2013). In Pakistan B. tabaci
has also been reported on 229 plant species
in cotton growing areas (Attique et al.,
2003) however weeds being unintended
plants that harbour whiteflies are the main
source of their carry over on crop plantings;
help in the dispersal of whitefly-transmitted
viruses (Bedford et al., 1998). Whitefly has
also potential to readily change their feeding
host plants and show variation in its food
preference (De Courcy Williams et al.,
1996).
Population dynamics of whitefly
The population of whitefly varies in
different seasons of the year depending upon
the atmospheric humidity, temperature and
rainfall (Horowitz et al., 1984; Horowitz,
1986; Rafiq et al., 2008). According to Latif
and Akhter, (2013) whitefly gradually
increased with environmental temperature,
humidity and suitability of feeding host
plant.
Impact of Climatic change on whitefly
12 Saghir et al
Study regarding influence of climate change
on population dynamics of B. tabaci are
important for accurate predictions and
improving management practices. Climate
change have various impacts on population
buildup as well as on biological parameters
of whitefly such as modified biological
parameters, reproductive patterns and
distribution due to rise in level of CO2 and
temperature. According to Levi et al.,
(2014) B. tabaci biotype B. Density was
observed at three different temperatures (25,
28 and 33°C) to determine its impacts on
life history parameters. Temperature
influenced oviposition, nymphal survival,
and reproduction rate of whitefly, with net
reproductive rates reducing to 36.4% at
33°C. They further explained that overall,
28°C was optimum temperature for whitefly
fitness and multiplication of whitefly was
between 28 and 33°C. increasing
temperature from optimum range had
negative impact on adult body size of both
male and female whitefly. So, climate
change directly influenced the life
parameters of pest as well as it induces
stress on the crop and under plant stress
conditions insect pest cause more losses than
on healthy plants (Holtzer et al., 1988;
Waring et al., 1992). Climate change also
had adverse effects on the
predatory/parasitism potential of bio-control
agents (Hance et al., 2007).
Virus transmission
Whitefly transmit Begomoviruses (Mayo
and Pringle, 1998) that caused crop losses
between 20 and 100% (Brown and Bird,
1992). Begomoviruses show yellow
mosaics, curling, stunting of leaf and vein
thickening symptoms (Cathrin and Ghanim,
2014). Mansoor et al. (1993) reported that
one million hectares were ruined in Pakistan
due to incidence of Cotton leaf curl virus.
13 Saghir et al
Life history of whitefly
Significant advances have been made in
understanding the biology, behavior,
ecology, population dynamics and pest
management strategy of this pest (Gerling
and Mayer, 1996). According to Gerling and
Horowitz (1986) developmental period of
whitefly ranged from 14-85 days during
summer and winter respectively.
Developmental rates were positively
correlated with day length but temperature
above 30–33°C was negatively correlated
with it. Females lived for 1 to 3 weeks
during summer but up to 2 months in winter.
Males were comparatively short lived for
less than 1 week only. Whitefly can rapidly
reproduce due to high reproductive rates
(Dittrich et al., 1990) and egg density per
female was reported 100-160 eggs (Gerling
and Horowitz, 1986).
Monitoring of whitefly
Assessment of whitefly population under
field condition is very useful to decide pest
management strategy. Ohnesorge and Rapp.
(1986) described a method for monitoring of
whitefly in which observations are recorded
from each of 24 plants in a field by
examining the lower side of top two leaves
and one leaf from the middle of the plant for
adult whiteflies. The total number of
whiteflies from all plants are then converted
to a mean count per plant. However George
(1986) reported the reasons behind increase
in population of B. tabaci that include:
Insecticide resistance, negative effects of
pesticides on beneficial fauna, favorable
climate and availability of host plants.
Natural enemies of whitefly
Beneficial insects play an important role in
the management of whitefly. In USA they
also initiated research on beneficial insects
for the management of Sweet potato
whitefly and they got success. For this
purpose: 5 years plan was initiated to
provide short and long term solution of the
problem. Main focus of research was on
introduction and conservation of biocontrol
agents. Amblyseius and Typhlodromus sp.,
Chrysoperla sp. were recorded feeding on B.
tabaci, similarly Encarsia and Eretmocerus
Parasitoids were able to cause high degree
of parasitism under low whitefly populations
(Dan Gerling, 1986; Hoddle et al., 1998).
Various other predators including
coccinellid beetles and predatory
mites (Amblyseius limonicus, A. swirskii
and Transeius montdorensis) have also been
found to be effective in controlling whitefly
(Heinz, 1996; Li et al., 2011; Cuthbertson,
2014). Similarly Hoelmer et al., 1998
14 Saghir et al
reported that a predator dusty wing,
Semidalis flinti Meindander (Neuroptera:
Coniopterygidae) in western USA, remained
very effective by consuming 2000 whitefly
eggs throughout its life under laboratory.
Biopesticides against whitefly
Other than beneficial insects some microbial
fauna has been reported in controlling
different stages of whitefly. Following
entomopathogenic organisms have shown
great effectiveness in controlling whitefly
populations likewise Isaria poprawskii
(Cabanillas et al., 2013), Lecanicillium
muscarium (Cuthbertson & Walters, 2005;
Cuthbertson et al., 2005; Cuthbertson et al.,
2005), Steinernema carpocapsae
(Cuthbertson et al., 2007), Steinernema
feltiae (Cuthbertson et al., 2003;
Cuthbertson et al., 2007). However control
failure of insect pests in the field may be
decreased due to environemental conditions,
timing, coverage and spray rates of bio-
pesticides/insecticides (Afzal et al. 2015)
Table 1: Use of microbial fauna against whitefly.
Biocontrol agent Pathogen References
Lecanicillium muscarium Fungus Cuthbertson & Walters, 2005; Cuthbertson et al., 2005
Isaria poprawskii Fungus Cabanillas et al., 2013
Lecanicillium muscarium Fungus Cuthbertson & Walters, 2005; Cuthbertson et al., 2005
Steinernema carpocapsae Nematode Cuthbertson et al., 2007
Steinernema feltiae Nematode Cuthbertson et al., 2003; Cuthbertson et al., 2007
Isaria poprawskii Fungus Cabanillas et al., 2013
Isaria fumosorosea Fungus
Chemical control of whitefly
Developing countries like Pakistan depend
heavily on chemical control against insect
pest in agriculture (Karunamoorthi et al.,
2012) because it is one of the best tool for
their management due to its quick action
(Khan et al., 2014). Organophosphate,
pyrethroid, and novel chemistry classes are
commonly used against various insect pests
of cotton (Afzal et al. 2015; Jan et al. 2015;
Ullah et al. 2016). Organophosphates are
acetyl cholinesterase enzyme inhibitors but
pyrethroids are modulators of sodium
channel and used for control of different
15 Saghir et al
insect pests of field crops in Pakistan
(Saleem et al., 2008). Neonicotinoids (e.g.,
acetamiprid and imidacloprid) are nicotinic
acetylcholine receptor agonists for the
control of sucking insectpests. Spinetoram
belongs to spinosyns that are fermented
products (Sparks et al., 1995). These
insecticides act as agonists of postsynaptic
cholinergic and (GABA) gated ion channels
(Young et al., 2003). Spinetoram has broad
insecticidal properties against both
hemipteran and homopteran insect pests
(Nauen et al. 2008). It is a lipid synthesis
inhibitor of acetyl CoA carboxylase to delay
development and egg laying capacity of
sucking pests (Bruck et al. 2009, Ramanaidu
and Cutler 2013). Generally, 6 to 10 sprays
have been reported on cotton during one
season (Ishtiaq et al. 2012) because 90% of
the farmers rely on chemical control for
protection against insect pest (Prayogo et al,
2005). The long term and over reliance on
insecticides to control insect pests exerted
strong selection pressure for evolution of
resistance (Tian et al., 2014). Previously,
different resistance levels against some
organophosphates and pyrethroids, has been
reported in field collected populations of
whitefly from Pakistan (Ullah et al. 2016).
In Pakistan B. tabaci remains active
throughout the year on various economical
crops, thus exposed continuously to
insecticides however growers apply more
insecticides on cotton than on vegetables
(Khan and Mehmood, 1999).
Cohen (1986) reported that early soil
treatment with insecticides was an effective
method for the management of whitefly.
Similarly Sharaf (1986) reported that ground
application of Amitraz was very effective in
controlling all nymphal stages of cotton
whitefly, Bemisia tabaci, however egg
exhibited more tolerance than the nymphal
and adult stage. He further explained that in
case of aerial application, its mixture with
endosulfan proved very effective against
whitefly. The first insecticides to control
whiteflies were of broad spectrum and
conventional applied singly or in mixtures of
OC’s, OP’s, carbamates and pyrethroids
known as cocktails (Leite et al., 1998). Due
to excessive use of insecticides against
whitefly (Palumbo et al. 2011) products
failed to control whitefly through
outstanding genetic capacity and
development of resistance to insecticides
(Perumal et al., 2009). Egg density per
female was 100-160 eggs but it was
increased to more than 300 eggs in
insecticide resistant strain in Sudan because
repeated pesticide applications resulted in
development of insecticide-resistant and
16 Saghir et al
high fecundated B. tabaci strain in the Sudan
(Gerling and Horowitz 1986).
Similarly Peregrine and Lemon (1986)
reported that a mixture of DDT and
dimethoate for the control of bollworms year
after year exerted a selection pressure on
whitefly that emerged itself from secondary
to primary pest of cotton. DDT also
stimulated whitefly fertility, increased egg
production and frequency of life cycles.
New chemistry insecticides likewise
neonicotinoids (imidacloprid, acetamiprid,
thiamethoxam, nitenpyram and thiacloprid)
and insect growth regulators (buprofezin and
pyriproxyfen) were manufactured and
included in insect pest management system.
Because in order to maintain the
sustainability of cotton production at long
terms, a better alternative to reliance of
pesticides is rational use of insecticides
(IGR’s) and integration of control strategies
as integrated pest management (IPM)
(Zalucki et al. 2009).
Use of sticky traps
Sticky traps are installed for inspection and
management of whitefly adult population by
visual counts (Ohnesorge and Rapp, 1986),
they are also useful to reduce the risk of
whitefly establishment on economic crops
(Cuthbertson and Vänninen, 2015).
Host plant resistance
Host plant resistance is an important
component of integrated pest management
strategy against insect pest of economic
crops. Meyerdirk and Coudriet (1986)
reported that B. tabaci is affected mainly by
morphological traits e.g., hairiness vs.
glabrousness, glandular trichomes, leaf
shapes (okra/super okra), microclimate due
to foliage density and the biochemical traits
of the leaf, e.g., pH of leaf sap. All these
characteristics constitute different
mechanisms of resistance. Varietal response
to whitefly population densities in different
crops has been observed and cultivars
exhibiting preference and non-preference
has also been recorded by Lambert et al.
(1995, 1997). Similarly viruses transmitted
by the whitefly, among cultivars also
demonstrated variations (Vieira
2009).Traditional resistance sources of
whitefly have been identified in different
crops and used successfully integrated pest
management system but development
of transgenically resistant crops through
genetic engineering are considered as a big
tool in future to overcome whitefly and
whitefly-transmitted viruses (Wilson et al.,
1993). In Pakistan also lot of work has been
done on host plant resistance.
17 Saghir et al
American experience regarding
management of cotton whitefly
Initiation of efforts included “sweetpotato
whitefly: 5 year plan for development of
management and control methodology”
during 1992. They started IPM projects
under community based action program for
the management of whitefly. This program
consisted of three pillars: Education- in
which growers learned about identification
of pest and its management in an integrated
way, Validation- in which pest monitoring
and effectiveness of its management
techniques were validated and
Implementation- in which actual monitoring,
control took place and further research
needed to improve it was also included
(Ellsworth et al., 1996).
Israeli experience regarding management
of cotton whitefly
Israeli experience showed that stabilization
of whitefly was due to existence of low
population of whitefly on many un-attended
weeds and ornamental plants from which it
spread on cotton crop. These weeds provide
food and shelter for the pest, therefore life
cycle of the pest remains continue
throughout the year even during off season
of the economic crop is available in the
field. Instead of weeds and ornamental
plants some other factors including natural
enemies, weather, water stress, production
technology and insecticide resistance also
have influence on the population of whitefly
(Gerling et al., 1996; Hoelmer, 1997).
Studies continuously conducted at various
aspects of whitefly completed by
Entomological group of Israel concluded
two general practices for the management of
whitefly (Gerling, 1980; Gerling and
Kravchenko, 1996; Horowitz and Ishaaya,
1996; Forer, 1990). First is restrictive use of
insecticides to specific stage of the crop,
second it is imperative to do one or at most
two spray of IGR (Pyriproxyfen) for the
management of whitefly. Research further
explained the theory and practice to record
sampling, pest biology and phenology,
importance and existence of natural enemies
and which chemicals can be safer for them
and delay buildup of resistance in pest
(Denholm et al., 1996; Naranjo et al., 1996;
Byrne and Blackmer, 1996; Riley et al.,
1996).
Risk of whitefly and future needs:
In cotton different biotypes are present in
different areas of cotton zones and needs to
study more on molecular basis in relation to
virus transition and w.fly biotypes in
different cotton growing areas. It is
recommended to focus on throughout season
18 Saghir et al
available predators i.e Orius bug and
Geocoris bug along with whitefly
parasitoids, Encarsia formosa and
Eretmocerus sp. They were found in all
cotton growing areas of south Punjab and
are effective whitefly predators in the field.
It is also suggested that mass rearing of
predators and parasitoids on large scale and
compatibility of safer insecticides with
beneficial insects is also inevitable to
include them in IPM module to protect
cotton from the increasing menace of
whitefly. It is also recommended that
insecticides used in previous studies are old
ones and new ones should be included for
better results and benefiting the farmers.
With the introduction of Bt population
dynamics and trend of whitefly on cotton
has been changed due to limited use of
pyrithroids against lepidopterous larvae,
therefore population dynamics should also
be updated. Studies on selection of effective
insecticides and monitoring of insecticide
resistance in whitefly/insectpest may be
included.
19 Saghir et al
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