Upload
others
View
2
Download
0
Embed Size (px)
Citation preview
30
3. Review of Literature
3.1. Major lepidopteran and mite pests of tea
The monographs by Green (1890) and Watt and Mann (1903) are the earliest
contributions on study of tea pests. Information on tea pests and their biology from
north-east India is subsequently given by Hainsworth (1952), Das (1965), Banerjee
(1983a, 1983b) and that of south India by Muraleedharan (1983). Present scenario of
insect and mite pests of tea throughout the world and their management has been
reviewed by Hazarika et al. (2009). Mukhopadhyay and Roy (2009) presented a recent
view on changing dimensions of climate, pest complex and pest management strategies
in sub Himalayan tea belt of North East India. Globally, 1031 arthropod species are
associated with tea (Chen and Chen, 1989). Due to the influence of climate, altitude,
nature of cultivation and age of plantation each geographic region may have its own
distinctive pest complex (Banerjee, 1983a; Muraleedharan, 1992; Anonymous, 1994;
Watt and Mann, 1903). In India only 300 species of insects belonging mainly to the
orders Lepidoptera, Hemiptera and Coleoptera, and mites (Acari) are recorded as tea
pests (Muraleedharan et al., 2001). Among these only 6 species are of major
importance from sub Himalayan West Bengal (Mukhopadhyay and Roy, 2009).
3.1.1. Major lepidopteran tea pests of Darjeeling Terai :
Among the tea attackers, the order Lepidoptera forms the largest group comprising
31.53% of the total pest species (Chen and Chen, 1989) and is enable to cause up to
40% crop loss (Banerjee, 1993). Recently even 100% crop loss by lepidopteran
defoliators is recorded in severely attacked sections of tea plantations of sub Himalayan
West Bengal (personal communication with tea estates). Major lepidopteran species
31
attacking tea in Terai and the Dooars regions of West Bengal are the species of looper
caterpillars, Buzura suppressaria, Hyposidra talaca and H. infixaria, belonging to the
family Geometridae (Anonymous, 1994; Mukhopadhyay and Roy, 2009). H. talaca
alone constitute 74% of the combined population of the lepidopterans attacking tea
(www.teaboard.gov.in). Some other members of the family Geometridae, such as,
Buzura bengaliaria, Boarmia sclenaria, B. acaciaria, Medasina strixaria, etc are
known to occur on tea, but none of them have attained the status of a pest (Anonymous,
1994). At the same time, some earlier known lepidopteran pests of tea, such as, jelly
grub, neetle grub etc. have lost their importance as pests. Some occasional and sporadic
lepidopteran pests of tea of Terai region include red slug caterpillars (Eterusia
magnifica), Ectropis bhurmitra, Cydia leucostoma, Caloptelia theivora, Ascotis sp.,
Euproctis latisfascia and others (Mukhopadhyay and Roy, 2009; Prasad and
Mukhopadhyay, 2013).
Buzura (Biston) suppressaria Guen.:
The common looper caterpillar, Buzura (Biston) suppressaria Guen., was first
recorded on tea in India by Cotes (1895) from Nowgong district of Assam. The
species had migrated to tea from jungle plants used as shade trees in the tea
plantations. Borthakur (1975) reported looper caterpillars as one of the important
pests of tea. Beeson (1941) in ‘The ecology and control of the forest insects of
India and neighboring countries’ recorded looper caterpillar on alternate hosts
such as Acacia modesta, A. catechu, Aleurites montana, Bauhinia variegata,
Cassia auriculata, Carissa diffusa, Dodonaea viscose, Lagerstroemia indica,
Dalbergia assamica, Deris robusta, Albizzia chinensis, A. odorotissima, A.
lebbek, Cajanus indicus and Priotropis cytisoides. By early 1990’s B.
suppressaria attained major pest status attacking tea in the plantations of Assam
and the Dooars region of West Bengal (Anonymous, 1994). However, in recent
32
past incidence of the species has become much lower than other loopers in Terai
region of West Bengal (Das, S. et al., 2010). Rare occurrence of looper
caterpillars has also been reported from tea growing areas of South India along
with their association with shade trees (Muraleedharan, 1991; 1993). Looper
caterpillars have been tainted as active defoliator of Indian and South-East Asian
tea (Hill, 1983).
Hyposidra talaca (Walker):
In recent past caterpillars of the geometrid species, Hyposidra talaca (Walker)
have emerged as major pest of tea from the Dooars region of West Bengal (Basu
Majumdar and Ghosh, 2004). Early report of occurrence of looper stages of H.
talaca on tea dates back to 1972, which also records the species on Cocoa,
Cinchona, Coffee and other fruit trees in tropical lowlands and highlads
(Entwistle, 1972). The species is polyphagous and is widely distributed. A brief
account on different species of Hyposidra is provided in the website,
www.mothsofborneo.com. Geographically, H. talaca is found in Indo-Australian
tropics from north-east Himalaya to Queensland and Solomons, and is recorded
from 96 plant species belonging to 28 plant families (Robinson et al., 2010) such
as Anacardiaceae (Anacardium sp.), Bombacaceae (Bombax sp.), Combretaceae
(Terminalia sp), Cupressaceae (Cupressus), Euphorbiaceae (Aleurites sp.,
Aporusa sp., Bischofia sp., Breynia sp., Glochidion sp., Manihot sp.), Moraceae
(Ficus sp.), Myrtaceae (Psidium sp.), Polygonaceae (Polygonum sp.), Rosaceae
(Rubus sp.), Rubiaceae (Cinchona sp., Coffea sp., Mussaenda sp.), Rutaceae
(Citrus sp., Euodia sp.), Sapindaceae (Schleichera sp.), Sterculiaceae
(Theobroma sp.), Theaceae (Camellia sp.), Verbenaceae (Tectona sp.) etc. to
name a few. The species is even found associated with narcotic plant coca
(Erythroxylum coca) (Rosen, 1991). The polyphagous species feeds on the foliage
33
of many forest trees in India (Mathew et al., 2005). Though about a hundred plant
species are recorded as alternate hosts of the species globally, it attained pest
status in a few cases. H. talaca is a quarantine pest of Litchi chinensis,
Dimocarpus longan and Garcinia mangostana from Thiland (Kuroko and
Lewvanich, 1993; Crop Protection Compendium (CPC), 2002; Thoda, 2004). It is
known as a pest of mango (Mangifera indica) (Butani, 1993; CPC, 2001) and
recently mentioned as a minor defoliator of forest trees, such as, Teak (Tectona
grandis) (Nair, 2007), Sal (Shoria robusta) (Sen Sharma and Thakur, 2008),
Quercus incana (Singh and Singh, 2004) etc. in India. H. talaca is also recorded
as a tea pest in Indonesia. Some work on the host association, biology and
oviposition behavior has been done by Das and Mukhopadhyay (2008), Das, S. et
al. (2010), Sinu et al. (2013).
Hyposidra infixaria Walker:
Different life stages (larva, pupa and adult) of H.infixaria apparently resemble
those of H.talaca, though distinguishing morphological features can be seen on
closer observation (Das, S. et al., 2010). H.infixaria is reported as a pest of tea in
West Bengal recently (Nair et al., 2008a; Das and Mukhopadhyay, 2009). The
occurrence of H. infixaria Walker ranges from north-east Himalaya to Taiwan and
Sundaland (www.mothsofborneo.com). The species had been reared on Pisum,
Desmos, Buchanania and Punica. Looper stage of the species was found
associated with castor bean, Ricinus communis and pomegranate, Punica
granatum and a weed, Rhodomyrtus tomentosa in Thiland (Winotai et al., 2005).
Nair et al. (2008a) reared the species on seven different host plants, wild jatropha,
jamun, tea, amra, jarul, citrus and water apple in Nadia district of West Bengal
and found lowest development period and highest growth index of the species on
34
tea. Difference in growth and survival of H. infixaria on different clonal varieties
of tea is also available (Basu Majumder et al., 2011).
3.1.2. Major mite pest of Darjeeling Terai:
Mites are persistent and the most serious pests of tea in almost all tea producing
countries (Cranham, 1966). Among twelve species of mites recorded on tea, the tea red
spider mite, Oligonychus coffeae Nietner (Acarina: Tetranychidae) is the major one and
is a serious pest of tea throughout the world (Banerjee, 1988; 1993) as well as in
Darjeeling Terai. O. coffeae was first discovered on tea in 1868 in Assam, India (Watt
and Mann, 1903) and besides India the mite is widely distributed in Bangladesh, Sri
Lanka, Taiwan, Burundi, Kenya, Malawai, Uganda, and Zimbabwe (Gotoh and Nagata,
2001).
Studies on life history and biology of O. coffeae on tea have been carried out in
different parts of the world including NE India (Das, 1959; Chakraborty et al., 2007;
Das et al., 2012; Mazid et al., 2013) and South India (Selvasundaram and
Muraleedharan, 2003; Muraleedharan et al., 2005). Recently, Roy et al. (2014) reviewed
the pest status, biology, ecology and management of O. coffeae in tea plantations.
The species inhabits upper leaf surface and are easily dislodged by heavy rainfall
(Hazarika et al., 2009). Life cycle of red spider mite, O. coffeae, consists of egg, larva,
nymph and adult stages. The egg is spherical with a curved filamentous process arising
from the upper pole and is red in colour, gradually changing to light orange before
hatching. Larva is six legged, almost round, yellowish at first which subsequently
change to pale orange. Nymphs are oval, eight legged and with deep reddish brown
abdomen. The adult female is somewhat elliptical; the posterior end of the abdomen is
broadly rounded and dark reddish brown in colour. The male is smaller with a narrower
abdomen tapering to the end (Fig. 3.1).
35
Fig. 3.1. Different stages of Oligonychus coffeae (red spider mite). 3.1a. Egg.
3.1b. Empty egg shells. 3.1c.Freshly hatched larva. 3.1d. Adult female
and male.
Leaf temperature and light penetration of tea bushes influence mite distribution
(Banerjee, 1979). Life cycle of red soider mite is dependent on temperature and relative
humidity (Das and Das, 1967). However, in their natural habitat other than abiotic
factors like temperature and relative humidity, the mite faces challenge from biotic
factors, such as, host plant and predators (Das et al., 2012). The optimal temperature for
growth and development is 30°C (Das and Das, 1967; Gotoh and Nagata, 2001). The
lower threshold for development is 10°C, and 232.6 degree days are required to
complete the life cycle from egg to egg (Gotoh and Nagata, 2001). The pest population
is found to be seasonally varying and dependent on the prevailing agroclimatic
conditions such as temperature and rainfall (Choudhury et al., 2006). In NE India, red
spider mite is found to be active and breed on tea throughout the year with highest
population density during late March and early April. Injury remains severe until the
monsoon rains wash off the active forms from the leaves (Das, 1959; Choudhury et al.,
♀
♂
3.1a
3.1b
3.1c 3.1d
36
2006; Mukhopadhyay and Roy, 2009). All stages of red spider mite persist on some of
the old leaves of un-pruned or skiffed tea bushes during cold weather and only a few
stay on clean pruned tea. It is the un-pruned tea fields that are primarily responsible for
the build up of red spider mite in spring (Das 1959). Though primarily a pest to tea, the
red spider mite is also known to attack jute, cotton, rubber, citrus, mango, oil palm and
many other tropical plants and weeds (Das, 1959). The mite has also been reported from
Deris robusta and Tephrosia candida in tea plantations of India (Andrews, 1928) and is
reported to attack Grevillea robusta and Albizzia falcata in Sri Lanka (Cranham, 1966).
Red spider mite of tea (O. coffeae) has gained economic importance because of crop
failure for a period of two or more months due to complete defoliation. It mainly attacks
the mature leaves, but under draught stress, tender leaves may also be attacked. Rao
(1974 a, 1974b) reported a loss of 340 – 511 kg of tea/ha due to red spider mite
infestation during draught. It causes considerable loss in tea production, the crop losses
ranging from 17 – 46% (Das, 1959, 1983; Lima et al., 1977; Mkwaila, 1983; Kilavuka,
1990).
3.2. Bio-ecology of polyphagous arthropod pests
The number of pestiferous species in agricultural crops is remarkably small in view of
the enormous pool of the potential invaders. Several biological characteristics of an
arthropod species, such as fecundity, diet breadth and voltinism, contribute to the
possibility of the species attaining pest status when a suitable habitat is made available
to it (Schoonhoven et al. 1998). Extensive bio-ecological studies enabled us to know
why among several dozen species or geographical subspecies of crucifer-feeding pierid
butterflies, only two species, Pieris brassicae and P. rapae have attained economic pest
status on crucifer crops worldwide. Among different aspects of bio-ecology, two
37
significant phenomena, host preference and post-embryonic development parameters,
which are important in the study of insect – plant interactions are discussed.
3.2.1. Host preference in polyphagous insects and mites:
Behavior is the link between physiology and ecology of animals (Bernays, 2001). Host
selection behavior of phytophagous insects is a catenary process, which is completed in
the acceptance of a plant suitable for oviposition and/or feeding (Schoonhoven, 1968).
An ability to use many plant species is an advantage. But at the same time, it is
suggested that generalist (polyphagous) insect herbivores find it relatively difficult to
choose among alternative host plants (for feeding or oviposition) due to neural
limitations giving rise to the problem of processing multiple sensory inputs (Levins and
Mac Arthur, 1969; Bernays, 2001), whereas a specialist (monophagous), who need not
to weigh among alternatives, is superior in detecting the appropriate host (Chapman et
al., 1981; Tingle et al., 1989). Studies on evolution of feeding pattern imply that
polyphagy may be ancestral to monophagy (Dethier, 1954; Bernays, 1998). In the order
Lepidoptera, the superfamilies Geometroidea and Noctuoidea have very high
proportions of generalists (Nielson and Common, 1991). In generalist lepidopterans and
other insect herbivores (except Orthopterans) different populations have relatively
restricted diets that are sometimes different in different regions such as in gypsy moth
(Fox and Morrow, 1981; Mauffette and Lechowicz, 1983). The term preference
involves a choice situation which relates a hierarchy of species of plants that can be
used as hosts (Thompson and Pellmyr, 1991). Exhibition of preference hierarchies for
host plants is common in polyphagous insects and it may be exercised by generalists if
they opt for the host species for supporting their development with varying success. In
addition to the substances of recognition (secondary plant metabolites), other conditions
provide a choice among viable hosts, such as the nitrogen content (White, 1984;
38
Bittencourt-Rodrigues and Zucoloto, 2005), the amount of attractive volatile substances
(Chew and Renwick, 1995), the plant physical characteristics (Bittencourt-Rodrigues
and Zucoloto, 2005) etc. However, changes in preference hierarchies through learning
can be favored for a variety of reasons such as variation of host quality or abundance
(Rausher, 1980; Papaj, 1986). Choice tests are simple and indispensable tool in any
insect-plant study including host preference (Schoonhoven et al., 2005). One of the
interesting aspects of insect feeding behavior is that feeding preference shows plasticity
(Ting and Hanson, 2002). In fact, it has often been reported in the entomological
literature that the food preferences of phytophagous insects can change following
feeding experience, such that the relative acceptability of plants already fed upon is
increased, i.e, induction of feeding preference occurs (Jermy et al., 1968; de Boer and
Hanson, 1984; Ting and Hanson, 2002). Most cases of such induced preference involve
minor changes; the food experienced becomes relatively more acceptable than
alternatives, although alternatives are also eaten (Szentesi and Jermy, 1990). In many
insect species, the induction of preference usually develops after one or more instars
remain on a particular host, with complex chemical stimuli participating in this process,
involving the central and peripheral nervous system (Hsiao, 1985). Host specific
phytochemical is found to modify chemoreceptors in Manduca sexta (del Campo et al.,
2001). Induction is quite common among lepidopteran larvae. Szentesi and Jermy
(1990) compiled examples of 22 lepidopterans and 12 insects belonging to other orders
where experience was found to change feeding preference. Other examples have since
been added to the list (Portillo et al., 1996; Ting and Hanson, 2002; Leal and Zucoloto,
2008). Induction of feeding preference due to experience has also been demonstrated in
mites such as two-spotted spider mite Tetranychus urticae (Gotoh et al., 1993; Egas and
Sabelis, 2001; Agrawal et al., 2002). Magowski et al. (2003) proposed associative
learning to be involved in the process of induction of feeding preference in T. urticae.
39
However, though induced preference is a fundamental type of behavioral change, it is
not universal among herbivores and could not be found in several insect species (Jermy,
1987; Sword and Chapman, 1994).
Schoonhoven et al. (2005) reviewed adaptive significance of induced feeding
preference. It has been assumed that it reflects an adaptation of insects in which
frequent changes of food type decreases the efficiency of food utilization. Induction
restricts the insect to the plant on which it is currently feeding (Ting and Hanson, 2002).
Restriction to a particular host plant following induction of feeding preference may lead
to evolution of host based biotypes in oligophagous/polyphagous insects and mites in
response to selection by the particular plant species (Mopper and Strauss, 1998; Ting
and Hanson, 2002). Formation of host-based biotypes are reported in many insects
belonging to different orders including lepidoptera and mite pests such as, peach-potato
aphid Myzus persicae (Hemiptera: Aphididae) (Saxena and Barrion, 1987), whitefly
Bemisia tabaci (Hemiptera: Aleyrodidae) (Baufeld and Unger, 1994; Cervera et al.,
2000), brown plant hopper Niliparvata lugens (Hemiptera: Delphacidae) (Saxena and
Barrion, 1987), European corn borer Ostrinia nubilalis (Lepidoptera: Pyralidae),
Walnut coddling moth Laspeyrsia pomonella (Lepidoptera: Tortricidae), red spider
mite Tetranychus urticae (Acarina: Tetranychidae) (Saxena and Barrion, 1987). The
entire panoply of evolutionary events form a spectrum, starting with ‘ecotypes’
(Thomas and Singer, 1998) and ‘biotypes’ (Eastop, 1973) at one extreme, passing
through races/strains, sub- and sibling species, and culminating in speciation itself
(Avise 1977, 1994, 2000).
40
3.2.2. Post- embryonic developmental parameters:
Environmental effects on phytophagous insects are largely exerted cumulatively
through their food (Safonkin, 2000). For successful feeding, the organism should be
capable of food assimilation and detoxification of some food components (Kondakova
and Strakhov, 1982; Rapport, 1988). So the study on the role of plants in adaptation of
phytophagous arthropod populations in a habitat is important.
Growth, development and reproduction of insects are strongly dependent on the quality
and quantity of food consumed (Scriber and Slansky, 1981). Variation in host-plant
quality may affect the body size of herbivorous insects which, in turn, can determine
life history traits, such as fecundity, longevity, and survival (Awmack and Leather,
2002; Saeed et al., 2010; Sequiera and Dixon, 1996). Post-embryonic development
period of an insect is an ideal parameter for interpreting the influence of its various
hosts. A good optimum diet results in faster postembryonic development. Previously
Naseri et al. (2009) examined life history and fecundity of Helicoverpa armigera on
different varieties of soybean. The data obtained in that study helped estimate the major
factors determining the susceptibility of soybean varieties. Farahani et al. (2011) studied
on the life table parameters of Spodoptera exigua and found that the development time
varied on different host plant. This observation is supported by the Azidah and Sofian-
Azirun (2006). Incubation period of eggs of Earias vitella varied considerably due to
host plant variation, which is shortest on Okra and longest in China rose (Syed et al.,
2011). Syed et al. (2011) also recorded considerable variation in the larval and pupal
period of E. vitella on different host plants, along with the adult longevity, fecundity
and life-cycle duration. Itoyama et al. (1999) found that the duration of the final larval
stadium of Spodoptera litura became significantly longer as diet quality decreased.
Delay in growth and development is an important symptom of feeding disturbances
41
(Levinson, 1976). Gypsy moth stands out as a study material in understanding the
complex mechanism of insect–host plant interactions in poly- and oligophagous
lepidopterans (Baranchikov, 1987). Host plant effect on gypsy moth performance and
its extremely polyphagous feeding habit have been well described. Host plant dependent
variation in larval growth and development is documented (Lazarević and Perić-
Mataruga, 2003). Larger body size is associated with higher fitness, i.e., higher
fecundity, flying and mating ability, stress tolerance, etc. Huge difference in body
weight was observed in Dectes taxanus when reared on different hosts. Higher adult
body weight could be correlated with female fecundity, male mating success and with
ability to survive adverse physical conditions (Michaud and Grant, 2005).
Polyphagous insects have the advantage that they can feed on different hosts that
provide different nutritional resources (Mozaffarian et al., 2007). The evolution of
polyphagy and its benefits have been studied in a number of insects (Sword and
Dopman, 1999; Bezerra et al., 2004). A number of studies on the biological parameters
of polyphagous lepidopteran pest of various crops, Spodoptera litura on different host
plants are done in India, Pakistan, China, Korea and other Asian countries. Larval
development of S. litura varied greatly depending on host plants, and the food
consumed by larva directly affected pupal size and weight (Xue et al., 2010a).
Parental nutrition may also affect population dynamics and trait evolution by
influencing quality of eggs. Researches on plastic responses to nutritive stress are
important for predicting insect outbreaks and understanding mechanisms of host plant
specialization. Presences of genotypic and phenotypic variations in natural populations
facilitate host-dependent specialization, host race formation and sympatric speciation in
herbivorous insects (Gorur, 2005). If host plant species constitute different selective
regimes to herbivorous insects, genetic differentiation and host plant-associated local
adaptation may occur (Ruiz-Monotoya et al., 2003). The existence of host-associated
42
populations has been examined in several insect pests (Downie et al., 2001; Abdullahi et
al., 2003; Sarafrazi et al., 2004).
3.3. Defense enzyme variability in populations of insects and
mites
Variation among populations may be caused by genetic factors, host plant and other
environmental influences (Agrawal et al., 2002). Toxic compounds ingested along with
the plant food can be hazardous, which the herbivores must overcome in order to
utilize the nutritional resources; another hazard results from exposure to pesticides used
for control of pest insects. Herbivorous species can tolerate these potentially toxic
compounds as they have evolved various physiological mechanisms to avoid their
harmful effects (Schoonhoven et al., 2005). They may either rapidly excrete the
unwanted compounds or degrade them through production of defense (=detoxification)
enzymes, or otherwise neutralize such chemicals before they can reach
pharmacologically active levels through development of target-site insensitivity
(Berenbaum et al., 1986; Brattsten, 1988a, 1988b). According to Yu (1986), enzyme
induction is a commonly occurring phenomenon representing an effective mechanism
of adaptation to external conditions. Some pesticides, especially insecticides and the
chemical constituents of host plants (plant secondary metabolites or allelochemicals), in
the case of phytophagous insects share a common metabolic detoxification process (Li
et al., 2007) and can have a great impact on inducing the enzymatic defense systems of
insects, thereby effecting insecticide resistance mechanisms (Yu, 1983, 1986; Zeng et
al., 2007). There are three major types of detoxification enzymes: 1) broad spectrum
oxidases such as mixed function oxidases or monoxygenases that include cytochrome P-
450 enzyme system, 2) hydrolases that break up esters, ethers and epoxides and 3)
conjugation systems such as glutathione S-transferase, which are mediated to cover up
43
the reactive part of the toxic chemical and further facilitate its removal. Major groups of
enzymes such as oxidases, hydrolases, transferases and reductases generally act in a
concerted way in the metabolism and conversion of foreign compounds to increasingly
polar metabolites in two arbitrary phases. Oxidation by cytochrome P450 dependent
monooxygenases and hydrolysis of ester bonds by carboxylesterases are conducted in
the phase I generating primary metabolites. Glutathione transferases are involved in
phase II conjugation reactions enabling conversion of primary metabolites into
secondary metabolites which are generally harmless.
Electrophoretic analysis of isozymes has contributed in the analysis of population
biology based on differences in geographic distribution, host plant association and
pesticide resistance status in many arthropod species (Loxdale and Hollander, 1989).
Esterase isozymes have been used in a number of insect population biology research,
for example, in Bemisia tabaci (Hemiptera: Aleyrodidae) (Guirao et al., 1997), Plutella
xylostella (Lepidoptera: Yponomeutidae) (Murai, 1993), Microtonus aethiopoides
(Hymenoptera: Braconidae) (Iline and Philips, 2003) etc. and are generally amongst the
most variable enzymes (Iline and Philips, 2003). Esterases also proved helpful in intra-
and inter-population variation studies in the mite, Tetranychus urticae (Acari:
Tetranychidae) (Goka and Takafuji, 1995a).
3.3.1. Host-based variability of defense enzymes:
Plants are suboptimal food due to inadequate nutrient ratios and the presence of
allelochemicals which the insect herbivores need to detoxify (Schoonhoven et al.,
1998). As herbivores are confronted by large amount of noxious chemicals in their plant
food, they literally are poisoned by every meal (Brattsten, 1979). Enzymatic
degradation of ingested plant toxic compounds by the herbivores is one of the
44
mechanisms to avoid their harmful effects. Herbivores, specially the polyphagous ones
have the opportunity to use several host plants as they can adapt to a heterogeneous
environment of diverse chemicals by efficient enzymatic detoxification mechanisms
(Ahmad et al., 1986). These enzymes are also known as ‘defense enzymes’ owing to the
protective role they play. Among these, variation of GST and GE in host-based
populations of arthropods, specially lepidopterans and mites is reviewed hereafter.
Variation of glutathione S- transferase (GST) and general esterase (GE)
enzymes in host-based populations of insects and mites:
Induction of GST by host plants has been reported by many authors. Yu (1982) reported
that in larval stages of fall armyworm, Spodoptera frugiperda reared on host plants,
such as, cowpeas, turnip and mustard, the activity of midgut GST was 7 – 10 fold higher
than the larvae of the same species reared on soybean, sorghum, millet, cucumber,
potato etc. In another polyphagous lepidopteran, Platynota idaeusalis, the tufted apple
bud moth, host plant affected activities of the detoxifying enzymes, glutathione
transferase and esterase (Dominguez-Gil and McPheron, 2000). Host plant mediated
variation in the activity of mid gut detoxification enzymes was also observed in larvae
of the eastern tiger swallowtail, Papilio glaucus glaucus when reared on leaves of black
cherry, tulip, paper birch, white ash or basswood with highest activity of GST and GE
activity on tulip and lowest on basswood leaves (Lindroth, 1989a). The same author
(1989b) suggested alteration in biochemical detoxification systems in evolutionary and
ecological adaptation of polyphagous luna moth, Actius luna to different food plants.
GST was found to be the key detoxification enzyme in metabolizing the chemical
components of sesame leaves in the larvae of S. litura as evident from a 6-fold increase
in GST level in the larvae fed with sesame leaves than those fed on an artificial diet
(Sintim et al. 2009). The success of polyphagous aphid pest, Myzus persicae to
different host plants has been related to the presence of enzymatic mechanisms of
45
detoxification responsible for the metabolisation of host-plant allelochemicals (Francis
et al. 2005; 2006). In a recent work by Cabrera-Brandt et al. (2010) a subspecies of
aphid, M. persicae nicotianae exhibited higher total esterase activities when reared on
tobacco than on pepper which suggested a participation of esterases on the ability of M.
persicae nicotianae to overcome the tobacco defenses. Mulin and Croft (1983) reported
host-related alterations of detoxification enzymes in the two spotted spider mite
Tetranychus urticae where these enzymes were stimulated by host plants such as carrot
and celery. Host based variation in the activity of esterase and GST in T. urticae is also
recorded by Yang et al. (2001) when they reared the species on lima bean, maize and
cucumber. Duration of host association is also found to influence the activities of these
enzymes in the mite species.
Pioneering research by Yu and co-workers could reveal specific role of an array of
allelochemicals in the induction of detoxification enzymes. The monoterpens (+)-α-
pinene, (-)-menthol and peppermint oil and the sesquiterpene lactone santonin were all
moderate inducers of the esterase, causing increases of 35 to 65 percent in activity in
fall armyworm larvae. The plant hormone analogs, (indole-3-acetonitrile and indole-3-
carbinol), as well as the flavonoids, (flavones and β-naphthoflavone), alkaloid (quinine),
along with furanocoumarin (xanthotoxin) stimulated the esterase, resulting in 35 to
114% increases of the enzyme (Yu and Hsu, 1985). Similar to this finding, plants such
as celery, potato and parsley were found active in inducing the esterase in the fall
armyworm larvae whereas corn, peanuts, cotton, soybeans, cowpeas, carrot, sweet
potato, peppermint, radish, turnip had no significant effect, thus reflecting the role of
host plant allelochemicals in inducing the hydrolase activity of the phytophag (Yu and
Hsu, 1985). Glutathione transferases also could metabolize toxic allelochemicals,
including α,β-unsaturated carbonyl compounds, isothiocyanates such as trans, trans-2,4-
decadienal, trans, trans-cinnamaldehyde, benzaldehyde, trans-2-hexenal, allyl
46
isothiocyanate, benzyl isothiocyanate and organothiocyanate such as benzyl
thiocyanate in lepidopterous insects (Wadleigh and Yu, 1987; 1988a; 1988b). The
glucosinolate, sinigrin, and the hydrolytic products of glucosinolates, β-
phenylethylisothiocyanate, indole 3-acetonitrile and indole 3-carbinol and flavones were
found to be potent inducers of the glutathione S-transferase in the armyworm (Yu,
1983). In addition, dietary coumarin and monoterpenes (α-pinene, β-pinene, limonene,
terpinene) induced GST in southern armyworm, Spodoptera eridania larvae (Brattsten
et al., 1984). However, monoterpenes were not inducers of transferase in fall armyworm
larvae (Yu 1982). Coumestrol, a coumerin analog found in a resistant soybean cultivar,
induced GST in soybean loopers (Rose et al., 1989). 2-Tridecanone found in wild
tomato leaves induced GST in tobacco budworm larvae (Riskallah et al., 1986).
Hemming and Lindroth (2000) studied the effects of phenolic glycosides on
detoxification activities of gypsy moth (Lymantria dispar) and forest tent caterpillar
(Malacosoma disstria) larvae. Esterase activities were induced by phenolic glycosides
only in gypsy moths, whereas GST activities were induced in both species. Ability to
detoxify phenolic glycosides enables these lepidopterans to adapt to such diet which is
otherwise toxic and unacceptable to folivores.
Apart from quantitative differences, electrophoretic variations in isoenzyme patterns
have also been documented in relation to host based populations of a particular species
of insects. Agarwala et al., (2002) could identify three host plant related clones of the
aphid, Lipaphis erysimi on the basis of variation in the banding pattern of esterase and
malic dehydrogenase. Electrophoretic pattern of esterase isozymes is used to study
variation in host- based populations of Bemisia tabaci (Wool et al., 1993; Helmi,
2010). Effect of host plants on the profile of detoxification enzymes of Helopeltis
theivora, a major sucking pest of tea could be documented through electrophoretic
analysis (Saha et al., 2012c).
47
3.3.2. Defense enzymes in pesticide-tolerant insect and mite
populations:
Applications of pesticides to control arthropod pests and vectors create selection
pressure on them leading to development of pesticide-tolerant and then pesticide-
resistant populations. Gene flow is an essential factor in spreading advantageous genes
such as pesticide-resistant genes in insect pests. Nearly 40 years of studies, all over the
world, suggest that, insecticide resistance could be correlated with quantitative and/or
qualitative changes in insecticide metabolizing enzymes. Efforts have been made to
estimate the activity of resistance associated enzyme with help of surrogate substrate,
whose products can be measured either in solution or cellulose filter paper or on
nitrocellulose membranes. Furthermore, these surrogate substrates can be used to probe
the isozymes and their mobility variance following electrophoresis and
electrofocussing. As stated earlier, there are three major types of detoxification
enzymes: 1) broad spectrum oxidases such as mixed function oxidases (MFOs) or
monoxygenases that include cytochrome P-450 (CYP450) enzyme system, 2)
hydrolases such as general esterases (GE) and 3) conjugation systems such as
glutathione S-transferases (GST). These three types of detoxification enzymes have
been documented to play a role selectively or in conjunction towards development of
resistance against different classes of insecticides in insects and mites, many of which
are of major pest status.
CYP450 dependent monoxygenases:
The CYP450 dependent monoxygenases are ubiquitous enzymes involved in
endogenous metabolism as well as metabolism of xenobiotics through oxidation
in phase I. CYP450 monoxygenase activities can be involved in the metabolism of
virtually all insecticides leading to an activation of the molecule or, more
48
generally to a detoxification and as a result may impart resistance to insecticides
(Feyerisen, 1999; Chen et al., 2005).
The role of GEs and GSTs as defense enzymes, the estimation of which has
mainly been done in the present thesis, are reviewed in details hereafter.
General esterases (GE) in insects:
GE are one the most significant enzymes in insects causing insecticide
detoxification in phase I metabolism. These defense enzyme groups have
repeatedly been implicated in metabolic resistance to the major organophosphate
(OP) and synthetic pyrethroids (SP) (Wheelock et al., 2005). OP and SP contain
carboxylester bonds that are subject to attack by esterase enzymes. Insect
carboxylesterases from the α-Esterase gene cluster is found to play an important
role in detoxification of OP insecticides (Jackson et al., 2013). Differences in
the amount of esterase activity between two strains of the same insect species is
considered as an indicator of the degree of sensitivity to certain insecticides,
subsequently, various biochemical assays have been used for insect populations
as possible indicators of insecticide resistance (Brown and Brogdon, 1987).
Several isozyme form of the esterases exist which can be detected by gel
electrophoresis. Besides higher production, change in electrophoretic banding
pattern such as occurrence of extra bands or bands with higher staining intensity
has been associated with resistance (Lalah et al., 1995; Neus et al., 2008). Role
of the GEs in imparting pesticide resistance in insects is summarized in table
3.1.
49
GST in insects:
GST is a family of multifunctional isozymes found in all eukaryotes. One of the
main functions of GST is to catalyze xenobiotics, including pesticides in the
marcapturic acid pathway leading to the elimination of toxic compounds (Hayes
and Pulford, 1995). In insects, this family of enzyme has been implicated as one
of the major factors in neutralizing the toxic effects of insecticides in phase II of
the metabolism process (Clark et al., 1986, Grant et al., 1991, Salinas and Wong,
1999). The majority of studies on insect GSTs have focused on their role in
detoxifying foreign compounds, in particular insecticides and plant
allelochemicals and more recently, their role in mediating oxidative stress
responses (Clark et al., 1986; Wang et al., 1991; Ranson et al., 2001; Vontas et
al., 2001; Sawicki et al., 2003). In insects, GST isozymes are present in three to
four forms in house flies (Clark and Dauterman 1982). Enhanced activities of
GSTs that confer insecticide resistance result from both quantitative and
qualitative alterations in gene expression (Chien et al., 1995; Wei et al., 2001).
There is evidence for over-expression of one or more GST isoforms in resistant
insects (Grant et al., 1991; Fournier et al., 1992; Marcombe et al., 2012). Role of
the GSTs in imparting pesticide resistance in insects is summarized in table 3.1.
50
Table 3.1. Insect pests showing enzyme-based (GE & GST) metabolic
resistance to insecticides (GE; general esterases and GST; glutathione S-
transferases)
Species of insect Resistant to Defense enzyme
imparting metabolic
resistance
Reference
Helicoverpa
armigera
SP GE
GST
Gunning et al., 1996;
Kranthi et al., 1997;
Achaleke et al., 2009; Wu
et al., 2011.
Omer et al., 2009
Plutella xylostella Malathione &
Phenthoate
SP
GE
GST
Chiang and Sun, 1993;
Maa and Liao, 2000
Dukare et al., 2009
Frankliniella
occidentalis
Methiocarb &
Acrinathin
GE Neus et al., 2008
Culex spp. OP GE Poirie et al., 1992;
Callaghan et al., 1994;
Jayawardena et al., 1994
Anopheles spp. Malathione
---
---
GE
GST
GST
Hemingway, 1982, 1983;
Herath and Davidson,
1981; Perera et al., 2008.
Ranson et al., 2001
Ganesh et al., 2003
Aedes aegypti OP, SP
---
GE
GST
Marcrombe et al., 2012
Grant et al., 1991;
Marcrombe et al., 2012
Musca domestica OP, SP
OP, SP, OC
GE
GST
Soderland and
Bloomquist, 1990; Funaki
et al., 1994
Oppenoorth et al.,1979;
Clark and Dauterman,
1982; Clark and Shaaman,
1984; Clark et al., 1986;
Fournier et al., 1992;
Chien et al., 1995; Wei et
al., 2001
51
Blattela germanica OP GE Valles, 1998
Myzus persicae OP, SP,
Carbamate
GE Davonshire and Field,
1991; 1995
Schizaphis
graminum
OP GE Ono et al., 1994; Zhu and
Gao, 1998; Zhu and He,
2000
Nilaparvata lugens SP GST Vontas et al., 2001
Oryzaephilus
surinamensis
Chlorpyriphos
---
GE
GST
Lee and Lees, 2001
Al-Dhaheri and Al-Deeb,
2012
Leptinotarsa
decemlineata
SP GE Argentine et al., 1995
Pediculus capitis Malathione GE Gao et al., 2005
Sitophilus oryzae OP, SP GE Iqbal et al., 2012 – 13
Bactocera
cucurbitae
OP, SP GE Rashid et al., 2012 – 13
Esterases and GSTs in mites:
Acaricides have been widely used for mite control in glasshouses, orchards and many
other cropping systems (Van Leeuwen et al., 2006). Frequent application of acaricides
to maintain mite populations below economic thresholds, as mites have a high
reproductive potential and extremely short life cycle. Such operations facilitate the
development of acaricide-resistance in them (Stumpf et al., 2001). Defense
(=detoxification) mechanisms to acaricides are also often attributed to enhanced activity
of defense enzymes, Esterases and GST. Higher Esterase and GST activities were
positively related with acaricide (OP and SP) resistance in two spotted spider mite, T.
urticae (Yang et al., 2001). Electrophoretic variations in Esterase-zymogram were
evident between abamectin resistant and susceptible T. urticae indicating possible
involvement of esterase-3 band in development of abamectin tolerance (Yorulmaz and
Ay, 2009). GSTs have been associated with macrocyclic lactone resistance in mites,
with elevated GST activity observed in abamectin resistant T. urticae (Konaz and
52
Nauen, 2004; Stumph and Nauen, 2002). Increased esterase and GST activity in
permethrin resistant Sarcoptes scabiei mite is reported (Pasay et al., 2009), of which,
GST appeared to be the most significant. Increased GST activity is associated with
permethrin tolerance in S. scabiei, GST inhibitors could restore susceptibility of the
mite species to permethrin and subsequently increased transcription of GST in
permethrin resistant S. scabiei was evident (Mounsey et al., 2010). Quantitative and
qualitative differences in esterase isozymes were recorded between pesticide-exposed
(tolerant) and unexposed (susceptible) populations of tea red spider mite, Oligonychus
coffeae from tea plantations of Terai region of West Bengal and South India (Sarker and
Mukhopadhyay, 2006b; Roobakkumar et al., 2012).
3.3.3. Host plants, defense enzymes and pesticide resistance: a
complex interrelation:
Host plants can modify the susceptibility of herbivorous arthropods to pesticides
(Brattsten, 1988a). A list some insect and mite crop pests that show host plant
dependent variation in the development of tolerance to pesticides is provided in Table
3.2. Physiological response of herbivores to host plants may lead to enhanced
metabolism of pesticides because underlying mechanisms that function in detoxification
of plant allelochemicals in their diets may also be effective in detoxifying pesticides
(Yang et al., 2001). Same set of defense enzymes, general esterases, GST and CYP450
dependent monooxygenase are involved in the metabolism of plant secondary chemicals
as well as pesticides in insect and mite systems. General esterases, which are capable of
degrading or sequestrating pesticides, can play a significant role in the detoxification of
OP and pyrethroid pesticides. Research works have demonstrated positive relation
between host-plant induced changes in defense enzyme level and susceptibility to
pesticides. Increased esterase level vis-á-vis tolerance in mite species T. urticae to
53
pesticide when using certain host plant species has been documented by Yang et al.
(2001). In S. litura higher esterase and GST activity on tobacco is correlated with higher
tolerance to several pesticides (Xue et al., 2010b). However, in tufted apple bud moth,
P. idaeusalis, though host plants could differentially induce detoxification enzymes,
patterns of enzyme activity and susceptibility to the pesticide azinphosmethyl could not
be clearly linked, inkling the complex relationship of the insect with the chemistry of its
host (Dominguez-Gil and McPheron, 2000).
Table 3.2. Changed pesticide susceptibility in arthropod-pests due to influence of
host plants
Species Reference
Aphis gossypii (Hemiptera) Furk et al., 1980; Godfray and Fuson,
2001
Myzus persicae (Hemiptera) Ambrose and Reghupathy, 1992
Nilaparvata lugens (Hemiptera) Heinrichs et al., 1984
Sogatella furcifera (Hemiptera) Heinrichs et al., 1984
Bemisia tabaci (Hemiptera) Castle et al., 2009; Liang et al., 2007; Xie
et al., 2010
Trialeurodes vaporariorum (Hemiptera) Liang et al., 2007
Leptinotarsa decemlineata (Coleoptera) Ghidiu et al., 1990; Mahdavi et al., 1991
Peridroma saucia (Lepidoptera) Berry et al., 1980
Spodoptera frugiperda (Lepidoptera) Wood et al., 1981
Heliothis armigera (Lepidoptera) Loganathan and Gopalan, 1985
Helicoverpa assulta (Lepidoptera) Wang et al., 2010
Epiphyas postvittana (Lepidoptera) Robertson et al., 1990
Spodoptera litura (Lepidoptera) Xue et al., 2010b
Tetranychus urticae (Acarina) Neiswander et al., 1950; Henneberry 1962;
Kady 1965; Gould et al., 1982; Yang et
al., 2001; Dermauw et al., 2012
54
3.4. Defense enzyme variability in insect and mite pests of tea in
North East India
In sub-Himalayan tea plantations of North-East India, most plantations are managed
conventionally by routine application of different organo-synthetic insecticides to
control pest populations. Organochlorines (OC), organophosphates (OP), synthetic
pyrethroids (SP) and neonicotinoids (NN)) are routinely applied round the year to keep
the insect pest populations under control (Sannigrahi and Talukdar, 2003;
Gurusubramanian et al., 2008). Repeated application of pesticides can result in the
resurgence of primary pests (Sivapalan, 1999), outbreak of secondary pest (Cranham,
1966) and development of resistance (Kawai, 1997; Roy et al., 2010a, 2010b). Many of
the tea pests being polyphagous feed on a number of plants besides tea, which indicate
that they can overcome challenge posed by a wide array of phytochemicals successfully.
There are evidences of physiological adaptation of some tea pests to both insecticides
and host plant chemicals involves induction of defense enzymes, such as, Esterases,
GST and Cytochrome P450 dependent monooxygenases (Saha et al. 2012a, 2012b,
2012c, Saha and Mukhopadhyay, 2013).
In recent days sucking insect pest, Helopeltis theivora has developed high tolerance to
some commonly used insecticides leading to control failures in sub Himalayan tea
plantations of West Bengal (Mukhopadhyay and Roy, 2009; Roy et al., 2011). Higher
levels of detoxifying enzyme (general esterases, GST and cytochrome P450
monooxygenase) activities in tea pests and their bearing on the level of susceptibility to
different synthetic insecticides have been documented (Sarker and Mukhopadhyay,
2006a; Saha et al., 2012a; Saha and Mukhopadhyay, 2013) from different sub-
Himalayan tea plantations of North-East India. There are reports of repeated control
failure of the sucking pests, E. flavescens and S.dorsalis in sub-Himalayan tea
55
plantations of North-East India. A positive relation to this effect has been established
between the population of the sucking pests showing high pesticide tolerance (LC50
values) and their titer of defense enzymes (Saha et al., 2012a; 2012b). Presence of
higher quantities of general esterases was reported in pesticide-exposed populations of
red slug caterpillar, Eterusia magnifica (Sarker and Mukhopadhyay, 2006a) and also in
tea red spider mite, Oligonychus coffeae (Sarker and Mukhopadhyay, 2006b).
Further, preliminary observations on difference in electrophoretic banding pattern of
general esterases in pesticide-exposed (field) population and pesticide-unexposed
(laboratory) population of the tea pests are available for red slug caterpillar, Eterusia
magnifica (Sarker and Mukhopadhyay, 2006a), tea mosquito bug, Helopeltis theivora
(Sarker and Mukhopadhyay, 2003) and tea red spider mite, Oligonychus coffeae (Sarker
and Mukhopadhyay, 2006b).
Host-based variation in H. theivora in terms of differential activity of three principal
xenobiotic detoxifying enzymes, the general esterases (GEs), glutathione S-transferases
(GSTs) and cytochrome P450 monooxygenases (CYPs) is documented (Saha et al.,
2012c). Further a host based differential activity of defense enzymes, esterases and GST
in tea looper pest H. talaca has also been observed (Das and Mukhopadhyay, 2008).
There are preliminary reports on the development of insecticide tolerance evident by
high LC values in H. talaca and H. infixaria (Nair et al., 2008b; Das, S. et al., 2010) and
in red spider mite, O. coffeae as well (Roy et al., 2008a; Roy et al., 2010a).
Literature on variability in defense enzymes in lepidopteran and mite pests of tea related
to their availability on different host plants or exposure to varying pesticides remains
scanty.