integrated management of plutella xylostella (lepidoptera
TRANSCRIPT
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Integrated management of Plutella xylostella (Lepidoptera: Plutellidae) in
vegetable growth tunnels
G Oberholzer
orcid.org 0000-0002-2257-879X
Dissertation accepted in fulfilment of the requirements for the degree Master of Science in Environmental Sciences with Integrated Pest Management at the North-West University
Supervisor: Prof MJ Du Plessis
Co-supervisor: Prof J Van den Berg
Graduation October 2019
24164763
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ACKNOWLEDGEMENTS
Dit is met ʼn hart vol dankbaarheid dat ek die volgende mense wil bedank vir al die
ondersteuning liefde en geduld deur my studies:
Aan Prof. Hannalene du Plessis en Prof. Johnnie Van den Berg baie dankie vir die
geleentheid en al die ondersteuning en raad deur die afgelope paar jaar dit word opreg
waardeer. Dankie dat julle ʼn liefde het vir wat julle doen en dat julle my daardie liefde
geleer het.
Aan my ouers, Nico en Renata Oberholzer, baie dankie vir die geleentheid wat julle vir
my gegee het ek sal julle ewig dankbaar wees. Julle is die definisie van perfekte ouers
en ek hoop ek kan eendag vir my kinders doen wat julle vir my gedoen het.
Aan my liewe sussie en swarrie baie dankie vir die ondersteuning, raad en laat aande
se werk. Sussie jy is iets besonders en ek is verby geseënd om jou in my lewe te kan
hê.
Aan Melana my engel dankie dat jy altyd daar was wanneer die werk te veel was en
wanneer ek net ʼn oor nodig gehad het. Jy is onbeskryflik, baie dankie vir die omgee liefde
baie koffie en moed in praat my lief dit is alles wat ek kon voor vra.
My vriende: Vir al die Caput manne wat altyd daar was vir my deur die koshuis dae dankie
vir die mense wat julle is ek waardeer elke liewe een se bydrae, veral Jako van Rooyen
my goeie vriend jy was altyd daar vir moed in praat en laat aande se werk dankie my
maat.
My vriende en kolegas by ECO–Rehab baie dankie vir julle ondersteuning en bydraes
deur my studies dit is onvervangbaar en baie spesiaal. Charlene Scott baie dankie vir jou
bydrae as vriendin en swot buddy vir meer as 6 jaar jy is n vriendin duisend.
Aan Pico–Gro en Erika Oberholzer baie dankie vir al die bystand van die nodige plante,
sade, populasies en nog vele meer dit word opreg waardeer.
Laastens my Hemelse Vader wat my die vermoë gegee het en al die mense in my lewe
geplaas het om my droom van ʼn meesters graad ʼn werklikheid te maak sonder U is niks
moontlik nie. Joh. 14:1 “Laat julle hart nie ontsteld word nie; glo in God, glo ook in My”.
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ABSTRACT
Plutella xylostella (L.) (Lepidoptera: Plutellidae) is a major pest on all Brassicaceae in
South Africa. Insecticide application is the main control strategy worldwide and concerns
are raised about the susceptibility of P. xylostella populations to insecticides in South
Africa. This concern sparked the investigation into other feasible control strategies and
measures mainly focused cultural control with trap crops. The objectives of this study
were to assess the following: feeding damage and percentage growth of P. xylostella on
selected host plants in no choice tests, the feeding preference of P. xylostella larvae on
selected host plants in two choice tests, the development and oviposition of P. xylostella
on selected host plants for possible use in a Push–Pull strategy and the susceptibility of
P. xylostella to selected insecticides. Five known P. xylostella host plant species were
selected, viz. pak–choi (Brassica rapa var. chinensis), cabbage (Brassica oleracea),
tatsoi (Brassica narinosa), kale (Brassica oleracea) and mustard (Brassica juncea). In the
two–choice tests conducted mustard was preferred for oviposition as well as feeding
preference by P. xylostella larvae. The fact that mustard was the preferred choice over
the other selected crops for oviposition and feeding preference makes it a viable
candidate for a trap crop for P. xylostella. Plutella xylostella populations were sampled
from two localities, Nelspruit (Mpumalanga province) and Bapsfontein (Gauteng
province). The toxicity of three insecticides used for control of P. xylostella in South Africa,
viz. lambda–cyhalothrin, flubendiamide and spinosad was estimated for both these
populations using an IRAC approved bioassay method. When comparing the
susceptibility of the two populations (Nelspruit (N2018–01) and Bapsfontein (B2018–01))
for lambda–cyhalothrin the LC80 values are higher (N2018–01: 9.35 and B2018–01 24.87)
than the recommended dosage of 8 ppm. Conversely, the selected populations (Nelspruit
and Bapsfontein) are highly susceptible to flubendiamide and spinosad with high mortality
levels > 80% with low dosages of 3 and 2 ppm respectively compared to the
recommended dosages of 48 and 216 ppm. The integration of trap crops and application
of insecticides with high efficacy of control of P. xylostella can contribute to reduce the
number of insecticide applications per season. It can also prolong the effective use of
these insecticides for control of P. xylostella in South Africa.
Keywords: Plutella xylostella, Brassicaceae, susceptibility, lambda–cyhalothrin, mustard
(Brassica juncea), bioassay, oviposition, feeding preference
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TABLE OF CONTENTS
ACKNOWLEDGEMENTS ................................................................................................ i
ABSTRACT ......................................................................................................................ii
Chapter 1: Introduction and literature review ................................................................... 1
1.1 Introduction ............................................................................................................ 1
1.2 Biology of Plutella xylostella .................................................................................. 2
1.3 Damage symptoms................................................................................................ 3
1.4 Distribution of Plutella xylostella ............................................................................ 3
1.5 Host preference ..................................................................................................... 5
1.6 Economic impact ................................................................................................... 6
1.7 Control of Plutella xylostella .................................................................................. 7
1.7.1 Cultural control .................................................................................................... 7
1.7.2 Biological control ................................................................................................. 9
1.7.3 Chemical control ................................................................................................ 10
1.8 Insecticide resistance .......................................................................................... 12
1.9 Resistance mechanisms in Plutella xylostella ..................................................... 18
1.10 Integrated Pest Management (IPM) ................................................................. 19
1.11 Aims and objectives ......................................................................................... 20
1.11.1 Aims ................................................................................................................ 20
1.11.2 Objectives........................................................................................................ 20
1.12 References ....................................................................................................... 21
Chapter 2: Cultural control of Plutella xylostella ............................................................ 42
2.1 Abstract ............................................................................................................... 42
2.2 Introduction ............................................................................................................. 43
2.2.1 Trap cropping ................................................................................................ 43
2.2.2 Pico–Gro test site .......................................................................................... 45
2.3 Material and methods .......................................................................................... 49
2.3.1 Plutella xylostella stock colony .......................................................................... 49
2.3.2 Larval feeding preference for selected Brassicas .............................................. 49
2.3.3 Larval feeding choice tests ................................................................................ 50
2.3.3.1 No–choice tests ........................................................................................... 50
2.3.3.2 Two–choice tests ......................................................................................... 51
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2.3.4 Oviposition preference tests .............................................................................. 52
2.3.5 Development time ............................................................................................. 52
2.3.6 Data Analysis .................................................................................................... 53
2.4 Results ................................................................................................................ 53
Choice tests .................................................................................................................. 53
2.4.1. No–choice tests ................................................................................................ 53
2.4.2 Two–choice tests ............................................................................................... 56
2.4.2.2 Mean percentage damage........................................................................... 58
2.4.2.3 Oviposition preference ................................................................................ 59
2.5 Discussion ........................................................................................................... 60
2.6 References .......................................................................................................... 63
Chapter 3: Susceptibility of Plutella xylostella populations to selected insecticides ...... 69
3.1 Abstract ............................................................................................................... 69
3.2 Introduction ............................................................................................................. 70
3.2.1 Insecticide resistance ........................................................................................ 71
3.2.2 Research and case studies ............................................................................... 72
3.3 Material and methods .......................................................................................... 75
3.3.1 Plutella xylostella sampling................................................................................ 75
3.3.2 Experimental design .......................................................................................... 75
3.3.3 Data Analysis .................................................................................................... 77
3.4 Results ................................................................................................................ 78
3.4.1 Spinosad ........................................................................................................... 78
3.4.2 Lambda–cyhalothrin .......................................................................................... 78
3.4.3 Flubendiamide ................................................................................................... 79
3.5 Discussion ........................................................................................................... 81
3.6 References .............................................................................................................. 83
Chapter 4: Conclusion and recommendations .............................................................. 88
4.1 Recommendations .............................................................................................. 90
4.2 References .............................................................................................................. 90
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Chapter 1: Introduction and literature review
1.1 Introduction
Brassicaceae is among the top 10 economically important plant families and includes a
diverse selection of 350 genera with over 3500 species (Warwick et al., 2003). Brassica
is a genus of plants in the mustard family and the members of the genus are collectively
known as cruciferous vegetables, cabbages, mustards and sometimes cole crops.
Brassicaceae are cultivated globally and includes Brassica oleracea (broccoli, cabbage,
kale, kohlrabi, Brussel sprouts and cauliflower), B. napus (rutabaga and rapeseed), B.
rapa (Chinese mustard, bok choy, turnip and Chinese cabbage), Raphanus sativus
(radish) and B. juncea (green mustard) (Warwick et al., 2003). Common types of brassica
used for food include cabbage, cauliflower, broccoli and Brussels sprouts (Warwick et al.,
2003). The main Brassicaceae crops that are grown in southern and eastern Africa
(Kenya, Uganda, Tanzania, Ethiopia, Mozambique, Zambia, Malawi, Zimbabwe and
South Africa) are cabbage, cauliflower, rape, kale and Chinese cabbage (Löhr and Gathu,
2002). Vegetables are grown mainly for local markets and supply vital minerals and
vitamins to mainly maize–based diets (Löhr and Gathu, 2002).
Between 1993 and 2009 the global area planted with Brassica vegetable crops increased
by 39% and in 2009 an estimated 3.4 million hectares were planted worldwide (FAO,
2012). From the cabbage (Brassica oleracea var. capitata L.) and other Brassica crops
cultivated in South Africa, an estimated 149 495 t was harvested in 2017 (FAO, 2017).
Associated with the global growth of Brassica vegetables was an intensification of farming
practices, with cabbage yields increasing by 27%, and Brassica vegetables were reported
to contribute more than US$26 billion to the world economy in 2012 (FAO, 2012).
Production constraints of Brassicaceae in Africa include insect pests, with the
Diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae) the most damaging
(Nyambo and Pekke, 1995). It is one of the most destructive and widespread pests of
Brassica vegetables globally, with annual control costs estimated to be billions of dollars
(Talekar, 1992; Shelton, 2004; Grzywacz et al., 2010; Zalucki et al., 2012). The earliest
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reports of P. xylostella in South Africa was in the early 1900’s (Gunn, 1917), with
economic losses to cruciferous crops recorded in Australia and South Africa (Muggeridge,
1930). The vast distribution of the pest is indicated by records on cruciferous crops
reported in at least 128 countries by 1972 (Salinas, 1972).
It may have its origin in Europe (Hardy, 1938), but Kfir (1998) speculated based on the
origin of its biocontrol agents (14 species of parasitoids) and host plants (175 species)
that it originated in South Africa. Several of the parasitoids of P. xylostella are known to
be endemic to South Africa, indicating a relationship between the diamondback moth and
the parasitoid species in this country (Kfir, 1998). The possibility that the diamondback
moth evolved on indigenous Brassicaceae in South Africa is highly possible. The large
number of indigenous Brassicaceae, the large diversity of parasitoids and the presence
of the well–known P. xylostella parasitoid, Diadegma collaris (Hymenoptera:
Ichneumonidae) all contribute to the notion that this pest may have originated in South
Africa (Kfir, 1998). Liu et al. (2000) used the same principles to argue that P. xylostella
originated in China but the number of parasitoids was not as significant as in South Africa.
1.2 Biology of Plutella xylostella
Plutella xylostella is multivoltine with four to 20 generations per year in temperate and
tropical regions, respectively (Harcourt, 1986; Vickers et al., 2004). This pest can also
reproduce in extreme climates due to its wide ecological tolerance (Chua and Lim, 1977).
A single P. xylostella female can lay more than 200 small oval, yellow eggs. The eggs are
0.5 mm in diameter and are laid singly or in clusters of up to four eggs mainly on the upper
leaf surface (Talekar et al., 1994; Justus et al., 2000). Eggs hatch after 4–8 days and first
instar larvae usually tunnel into the spongy mesophyll tissues of leaves (Harcourt, 1957).
Second, third and fourth instar larvae are surface feeders and consume leaves, buds,
flowers, siliques, the green outer layer of stems and also developing seeds within older
siliques (Harcourt, 1957). The fourth and fifth instar larvae are active feeders and the
mature larva spins a delicate cocoon that is attached at each end to the leaf. Inside the
cocoon a prepupal phase precedes pupation and the green larva turns brown (Harcourt,
1957). A moth emerges from the pupa in the cocoon. Successful development can occur
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at constant temperatures from 8 to 32 °C and under alternating regimes between 4 °C to
38 °C (Liu et al., 2002). Development from egg to adult takes approximately 14 days in
the summer under field conditions in South Africa, with 4–6 generations per year
(Harcourt, 1957). Plutella xylostella is active year–round in South Africa with development
slowing down in winter (Annecke and Moran, 1982). There is no diapause or dormancy
period in areas where year–round reproduction occurs (Robertson, 1939).
1.3 Damage symptoms
Plutella xylostella larvae feed on the leaf surface leaving only the epidermis intact where
low to medium infestation levels occur (Talekar and Shelton, 1993). The larvae and pupae
can be found near damaged leaves especially in tight spaces where leaves and veins
join. In heavily infested plants, entire leaves can be destroyed leaving only the veins
behind (Talekar and Shelton, 1993). Damage is usually first seen on the edges of fields
and the infested plants look stunted and die if left untreated (Talekar and Shelton, 1993).
1.4 Distribution of Plutella xylostella
Plutella xylostella is present wherever its host plants occur and it is considered the most
widely distributed of all lepidopteran species (Shelton, 2004). Despite its pest status and
distribution, little is known about its abundance and global distribution (Zalucki and
Furlong, 2011). Based on how P. xylostella responds to climate, Zalucki and Furlong
(2011) published a bioclimatic model and a map indicating the areas suitable for
permanent occupation as well as for seasonal reproduction and population growth (Figure
1.1). Infestations are usually most severe in the tropics and sub–tropics where Brassicas
are cultivated year–round (Shelton, 2004). These are also the areas indicated by the
abovementioned model to be climatically the most suitable for P. xylostella persistence.
The infestation levels do, however, vary between seasons and locations depending on
the natural enemies present, migration, overwintering populations and preventative
control strategies (Shelton, 2004).
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Figure 1.1: Climate suitability for Plutella xylostella. The Ecoclimatic Index (EI) describes
the potential suitability for persistence and the growth index (GI), the suitability for
seasonal reproduction and population growth (Zalucki and Furlong, 2011).
The dispersal ability of P. xylostella affects and enhances its global distribution and pest
status. The moths disperse through air convection currents over national borders
(Bretherton, 1982). Seasonal moth migrations were reported in Scotland, Canada and
China (Talekar and Shelton, 1993; Chapman et al., 2002). Immature stages such as eggs
and pupae can be dispersed by the wind (Chapman et al., 2002) and the pest is
transported from one region to another with Brassicaceae seedlings containing larvae
and eggs. Plant material left behind after harvest and moved to a refuse area can also
contain larvae and eggs that can infest other plants nearby (Chapman et al., 2002).
Plutella xylostella moths move within crops by short flights between plants (Mo et al.,
2003). Dispersal of male and female moths are similar with 90% of them traveling less
than 100 m within a week from release (Mo et al., 2003). Less than 1% of individuals
move vast distances (> 1km) to neighbouring fields for reproduction (Mo et al., 2003).
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1.5 Host preference
The host plant range for P. xylostella is largely restricted to Brassicaceae (Sarfraz et al.,
2006). However, Zhang et al. (2007) reported oviposition on non–host plants not
belonging to the Brassicaceae. The only example of non–host oviposition is on snow pea,
Pisum sativum var. saccharatum (Fabales) and sugar–snap pea P. sativum var.
macrocarpon (Fabales) (Rossbach et al., 2006) in Kenya. Survival on P. sativum was
enabled by certain alleles but they were not fixed, which indicated genetic variance of P.
xylostella and not a host shift (Löhr and Rossbach, 2004; Henniges–Jassen et al., 2011).
Plutella xylostella moths use olfactory cues rather than vision as the main means to locate
host plants at short distances (Pivnick et al., 1994). Chemical cues are used upon landing
to establish host plant and oviposition sites (Justus and Mitchell, 1996). The distribution
within a crop field is usually irregular for vegetable crops (Waters et al., 2009). The
reasons behind the sporadic distribution are nutrient levels of hosts, field size, variation
in plant morphology and chemistry and feeding damage by other pests (Waters et al.,
2009; Hambäck et al., 2010; Sarfraz et al., 2010; Kos et al., 2011).
Brassicaceae species have developed diverse defence mechanisms against herbivory
which includes chemical and mechanical traits (Karowe and Grubb, 2011). Thick cuticles
enable defence against herbivores in some species of mustard such as Arabidopsis
thaliana and Lepidium sativum (Karowe and Grubb, 2011). Brassica oleracea reacts to
herbivory with the production of glucosinolates, which is regulated by jasmonic acid levels
(Tytgat et al., 2013). Brassica nigra (black mustard) developed enlarged trichomes, and
higher concentrations of glucosinolates in more valuable plant parts such as flowers
(Traw and Feeny, 2008). Glucosinolates are non–volatile composites that control host
plant interactions (Tang et al., 1997). Plutella xylostella is able to overcome both saponins
and glucosinolates, defence compounds against insects (Ratzka et al., 2002; Himanen et
al., 2009). Glucosinolates are limited in their biological activity and only play a role when
plant material is damaged (Hopkins et al., 2009). The damaged plant material causes
glucosinolates to be exposed to myrosinase, resulting in the production of hydrolysis
products, which is toxic to herbivorous insects (Li et al., 2000). These toxic products
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include isothiocyanates, a wide spectrum toxin for insects, including P. xylostella (Li et
al., 2000). The production of isothiocyanates is avoided in P. xylostella by a glucosinolate
sulfatase in the lumen of the larval gut, which eliminates sulfur from glucosinolate
molecules, causing myrosinase hydrolysis and preventing the formation of toxins (Ratzka
et al., 2002). The high amounts of glucosinolate sulphatase in the P. xylostella gut causes
the toxic compounds to be ineffective by converting glucosinolates into desulpho–
glucosinolates (Ratzka et al., 2002). Plutella xylostella ingests glucosinolates with minimal
effect on their performance (Ratzka et al., 2002). Isothiocyanates can function as both
oviposition stimulants and attractants (Renwick et al., 2006). Plutella xylostella also rely
on these compounds for host location (Sarfraz et al., 2006). Some Barbarea species
contain glucosinolates in their surface waxes, which explains their attractiveness for P.
xylostella females for oviposition (Shelton and Badenes–Perez, 2008). Although
glucosinolates attract P. xylostella, these compounds are also related to lower weight and
growth rates at different life stages (Li et al., 2000; Sun et al., 2009) and affect fitness
(Badenes–Perez et al., 2014).
The incidence of P. xylostella infestation in cruciferous vegetables is determined by the
number of larvae present in a pre–defined area (Berry, 2000). Various traps can also be
used to aid in the detection of P. xylostella in fields. The economic threshold for P.
xylostella on cabbage crops is 37 larvae/10 plants (Jusoh et al., 1982).
1.6 Economic impact
Plutella xylostella is regarded as the most destructive pest of Brassicas worldwide with
crop losses up to 90% (Verkek and Wright, 1996). The global economic impact of P.
xylostella is difficult to establish due to the diverse range of farm sizes as well as the
range of cruciferous production areas worldwide (Zalucki et al., 2012). Schelhorn et al.
(2008) estimated the global direct loss spent on control of P. xylostella to be US$ 1 billion.
A more recent estimate amounts to US$4–5 billion, if yield losses and control cost for all
Brassicas are taken into account (Zalucki et al., 2012; Bradshaw et al., 2016). Crop loss
in smallholder cabbage production systems caused by P. xylostella is estimated at 31%
(Macharia et al., 2013), but if this pest is left uncontrolled crop losses can reach 100%
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(Ayalew, 2006). Small–scale farmers in southern Africa experience up to 90% defoliation
of their crops regardless of the growth stage of Brassicas (Machekano et al., 2017).
South Africa exports Brassicas to various countries in Africa including Zambia, Lesotho,
Swaziland, Namibia, Angola, Botswana and Mozambique (South African Department of
Agriculture, 2014). Global demands for organic vegetables have significantly grown with
new markets opening up for African economies if high quality and standards can be met
(Lubinga et al., 2014). Plutella xylostella can have a negative influence on the
opportunities in these new markets (Lubinga et al., 2014).
1.7 Control of Plutella xylostella
Despite the efforts to establish integrated pest management programs, control strategies
rely mainly on insecticide application (Grzywacz et al., 2010). Other control strategies
include cultural and biological control (Shelton and Nault, 2004). The high pest status of
P. xylostella can mainly be attributed to insecticide resistance and the absence of natural
enemies in the areas where host crops are cultivated (Talker and Shelton, 1993).
1.7.1 Cultural control
Cultural control is important in establishing a long–term control strategy for P. xylostella
(Diez et al., 2012). Many studies focused on using plants or certain plant characteristics
to control insect pests (Boiça Júnior et al., 2013; Girão Filho et al., 2014). Plants have
specific modes of action in terms of their defence against various insect pests, which
include repellence, toxicity, growth regulation, oviposition inhibition and feeding
deterrence (Maia and Moore, 2011; Liang et al., 2012; Amoabeng et al., 2014).
Resistance development to insecticides by P. xylostella (Tabashnik et al., 1990; Shelton
et al., 1993; Zhao et al., 2002) in combination with food safety have motivated the
development of alternative management strategies using trap crops (Hooks and Johnson,
2003; Shelton and Badenes–Perez, 2006). Trap crops are plants cultivated to attract
insects and other organisms to protect the main crop against pest attack (Heikki and
Hokkanen, 1991). Trap crops are less economically important plants that are highly
preferred by P. xylostella which are planted between the Brassicas of choice in a
8
commercial field (Shelton and Nault, 2004). Protection is attained by either converging
the pest to a certain area or inhibiting the pest from reaching the main crop (Heikki and
Hokkanen, 1991). All pests prefer particular plants, which include different cultivars,
species and stages (Heikki and Hokkanen, 1991). For a trap crop to be effective in
reducing P. xylostella populations, the trap crop has to be in the vegetative stage and
healthy (Shelton and Nault, 2004) and should be available the entire growing season of
a commercial crop (Heikki and Hokkanen, 1991). The use of trap crops to control P.
xylostella has been attempted more than for any other insect pest with varying results
(Shelton and Badenes–Perez, 2006; Nethononda et al., 2016). Only a few of these were
applied to small scale testing or field experiments with no full–scale implementation of a
trap crop (Shelton and Badenes–Perez, 2006).
Additional reasons to implement trap crops are the environmental and economic benefits
related to this control strategy (Heikki and Hokkanen, 1991). Trap crop implementation
can reduce the costs of chemical control to a level compensating for the implementation
cost of the trap crops (Swezey and Daxl, 1988). Yields are also higher in trap crop
systems than in conventional fields (Hokkanen et al., 1986). Since the main crop does
not need excessive insecticide application in a trap cropping system, natural enemies are
left unharmed. Trap cropping can also attract and increase the incidence of natural
enemies and consequently biological control of the target species in the cultivated area
(Heikki and Hokkanen, 1991). This method is used successfully in the Soviet Union to
protect cabbage (Adashkevich, 1974; Vorotintseva, 1974; AI–Hitty and Sharif, 1987).
Trap crop implementation is negatively affected by farmers not willing to cultivate trap
crops with no market value (Khan et al., 2007). Other pests of the main crop such as
aphids can take refuge in the trap crop, when considering P. xylostella as the main pest
(Nofemela, 2008). Inconsistent results of trap crops are also problematic (Shelton and
Badenes–Perez, 2006).
The most proposed trap crops for P. xylostella is yellow rocket (Barbarea vulgaris)
(Brassicaceae) and Indian mustard (Brassica juncea juncea) (Brassicaceae) (Charleston
and Kfir, 2000; Badenes–Perez et al., 2004; Lu et al., 2004; Shelton and Nault, 2004;
9
Badenes–Perez et al., 2005). Yellow rocket is a biannual invasive weed that occurs
worldwide in temperate regions (Uva et al., 1997). Plutella xylostella moths prefer yellow
rocket as an oviposition substrate but it is not preferred by the larvae for feeding and larval
survival on yellow rocket is low (Sarfraz et al., 2006). Yellow rocket could therefore be
regarded as a dead–end trap crop. Dead–end trap crops are specific plant species, which
is highly preferred for oviposition with low larval fitness which can serve as a replacement
for conventional insecticides (Sarfraz et al., 2006).
Barbarea vulgaris deters feeding by P. xylostella larvae by means of triterpenoid saponins
3–0–b–cellobiosyloleanolic acid (saponin 2) and 3–0–b–cellobiosylhederagenin (saponin
1) (Badenes–Perez et al., 2010). Saponins are also cyto–toxic to P. xylostella cells
through the cell membrane, which is being permeated to induce apoptosis (De Geyter et
al., 2012). There are two morphological forms of B. vulgaris var. arcuatea, pubescent (P)
containing hairs and glabrous (G) being hairless. The two forms differ strongly in saponin
and glucosinolates content and in terms of genetics (Augustin et al., 2012). Plutella
xylostella larvae do not survive on G–type B. vulgaris var. arcuata due to saponins 1 and
2 being present (Badenes–Perez et al., 2010). P–type B. vulgaris var. arcuata contains
saponins, but P. xylostella larvae survive due to saponins 1 and 2 being absent (Kuzina
et al., 2011). Barbarea vulgaris var. variegate, resistant to P. xylostella larvae, similarly
contains saponins 1 and 2 (Badenes–Perez et al., 2011).
There are contradictions in reports from different parts of the world on the use of Indian
mustard as a trap crop. In South Africa, this species showed potential as a trap crop
although it has no specific advantages to cabbage production in particular (Charleston
and Kfir, 2000). This is in contrast to results from Indonesia where no effective control of
P. xylostella was achieved with Indian mustard (Omoy et al., 1995).
1.7.2 Biological control
Successful biological control programs depend mainly on the correct identification of
natural control agents (Collier and Steenwyk, 2004). Correct timing is essential since
biocontrol agents that colonize P. xylostella infested crops late in the season may not
provide effective control (Collier and Steenwyk, 2004). The controlled release of a high
10
number of natural enemies may provide effective biological control of this pest (Collier
and Steenwyk, 2004). However, the release of low numbers of biocontrol agents early in
the season allows for the establishment of a successful biocontrol agent population.
These agents can then provide pest control later in the season. This approach can be
effective in an area where P. xylostella overwinters and cause predictable damage later
in the season (Collier and Steenwyk, 2004).
Various natural enemies can suppress P. xylostella. It is reported that there are various
parasitoid species that attack the different stages of P. xylostella globally (Delvare, 2004).
These parasitoids can be grouped into 38 larval, six egg and 13 pupal parasitoids (Lim,
1986; Talekar and Shelton, 1993). Trichogramma and Trichogrammatoidea
(Hymenoptera: Trichogrammatidae) parasitoids are not well established bio–control
agents since egg parasitoids are not always host–specific and parasitize non–target
species (Talekar and Shelton, 1993). The best control by parasitoids is therefore from
larval parasitoids (Goulet and Huber, 1993). The genera Cotesia (Braconidae), Microplitis
(Braconidae) and Diadegma (Ichneumonidae) are the most effective parasitoids for P.
xylostella control (Hardy, 1938, Liu et al., 2000).
Biologically based efforts to control P. xylostella in Africa and Asia have focused strongly
on parasitoid introductions. However, the identification and deployment of promising
parasitoids in many regions, have had limited impact, due to insecticide applications
(Grzywacz et al., 2010). Studies done in Kenya, Uganda, Tanzania, Mozambique,
Zambia, Malawi and Zimbabwe reported low levels of parasitism by Oomyzus sokolowskii
(Kurdjimov) and Diadegma spp. (Löhr and Gathu, 2002). Diadegma is the most
widespread and effective parasitoid genus parasitising P. xylostella in Uganda, Kenya,
Tanzania and South Africa (Kfir, 1997; Seif and Löhr 1998). Diadegma collaris was
identified as a potential parasitoid for control of P. xylostella in East Africa since it is
commonly found in southern Africa (Kfir, 1997; Löhr and Gathu, 2002).
1.7.3 Chemical control
Information on chemical control of P. xylostella by farmers in South Africa is limited (Table
1.1) (Furlong et al., 2013), although these farmers rely completely on insecticides for
control of P. xylostella (Canico et al., 2013). Compared to global standards, maximum
11
application rates and frequencies are not adhered to by southern African farmers
(Williamson et al., 2008). In Botswana, most pesticides are applied at a rate of between
1 to10 fold greater than the recommended dosage rates (Machekano et al., 2019).
Organophosphates are applied at 1 to 3 fold and pyrethroids at 5 to10 fold the
recommended rate (Machekano et al., 2019). Frequency of application can vary from
once a month to more than three times a week (Obopile et al., 2008; Harvey, 2015). In
Botswana, 41 active ingredients sold under 56 trade names from 17 chemical groups, are
used to control P. xylostella (Machekano et al., 2019). Wandaat and Kugbe (2015)
reported that farmers use at least two to six alternating insecticides in southern Africa.
However, Ngowi et al. (2007), reported that up to five insecticides are mixed in a single
application without any recommendation of agro–chemical companies. It can result in
undesirable chemical reactions, phytotoxicity and longer withholding periods for the
respective insecticides (Baliga and Repetto, 1996). Uncontrolled use of insecticides
contributes to the increased cases of resistance and destruction of biological control
populations (Safraz et al., 2005; Grzywacz et al., 2010; Furlong et al., 2013).
Table 1.1: Insecticides and rates used for Plutella xylostella control on cabbage at six
sites in South Africa (Sereda et al., 1997).
Area Application
frequency
Insecticides Recommended
dosage (RD)
Brits Weekly Chlorpyrifos
Cypermethrin
Parathion
4xRD
RD
RD
Bloemfontein 1 Weekly Deltamethrin
Methamidophos
Parathion
Mevinphos
Betacyfluthrin
Bacillus thuringiensis var. kursaki
RD
RD
RD
RD
RD
RD
12
1.8 Insecticide resistance
Whalon and McGaughey (1998) defined resistance as an evolutionary process where
genetic adaptation is caused by biocide selection causing unsuccessful control. Plutella
xylostella is controlled mainly with insecticides in South Africa as in many other countries
(Mosiane et al., 2003). There are three reasons for the intensive insecticide application
on Brassicaceae crops (Sarfraz and Keddie, 2005). Firstly, insecticides are applied to
control P. xylostella, but it also kills the natural enemies and subsequent continued use
of selected insecticides results in resistance evolution and unsuccessful control (Sayyed
et al., 2002). Secondly, the highly migratory moths may migrate to areas with no natural
Bloemfontein 2 Twice a week Deltamethrin
Parathion
Betacyfluthrin
Bacillus thuringiensis var. kursaki
Methamidophos
RD
RD
RD
RD
RD
Ventersdorp Every 3–4 days Parathion
Methamidophos
Chlorpyrifos
Lambda–cyhalothrin
RD
RD
RD
RD
Skeerpoort Every 7–10 days Chlorpyrifos
Cypermethrin
Dimethoate
Pyrol
11xRD
16xRD
8xRD
RD
Roodeplaat 3 applications a
season
Mevinphos
Parathion
Carbofuran
RD
RD
RD
13
biological control agents resulting in insecticide applications (Chapman et al., 2002;
Sarfraz and Keddie, 2005). Thirdly, markets prescribe produce to meet certain standards,
which have an influence on control strategies, with farmers relying on insecticides for
effective control (Sarfraz and Keddie, 2005). Market pressure in Asia results in cabbage
farmers applying insecticides at least every 3–5 days with 12–16 applications in one
season (Shamsudin et al., 2004). The result of overusing insecticides is evident in the last
100 years where more than 500 insect species have developed resistance to selected
insecticides (Mota–Sanchez et al., 2002).
Plutella xylostella was the first crop pest to become resistant to DDT in the mid 1900’s
(Ankersmit, 1953) and also the first insect pest with resistance to Bacillus thuringiensis
(Tabashnik et al., 1990). By 2011, P. xylostella showed resistance to most insecticides
applied under field conditions in certain cropping areas (Ridland and Endersby, 2011)
and also to new insecticide groups, including diamides, spinosyns and phenylpyrazoles
(Table 1.2) (Gong et al., 2014). Worldwide P. xylostella is resistant to 91 active ingredients
from various modes of actions including 12 strains of B. thuringiensis (Bt) (Xia et al., 2014;
Legwaila et al., 2014). When comparing insecticide resistance for P. xylostella in southern
Africa to statistics from the rest of the world, southern Africa has a relatively low number
of reports (IRAC, 2015). Farmers who keep using the same active ingredient and apply
insecticides more frequently with an increase in dosage rates or as a mixture of various
insecticides promote resistant populations of P. xylostella (Ngowi et al., 2007; Canico et
al., 2013).
Table 1.2: Insecticide resistance of P. xylostella reported in Brassica producing areas in
2005 (Sarfraz and Keddie, 2005).
Area Insecticide Group Resistance
ratio (RR)
Reference
South
Carolina
Cry1C Bt 63 100 Zhao et al. (2000).
Malaysia Spinosad Spinosyns 20 600 Sayyed et al. (2004)
14
Abamectin Avermectins 16 300 Sayyed et al. (2004)
Fipronil Phenylpyrazoles 70 Sayyed et al. (2004)
Cry1 Ac Bt 1680 Sayyed et al. (2004)
Japan Acetamiprid Neonicotinoids 110 Ninsin (2004)
Hawaii Spinosad Spinosyns 1340 Mau and Gusukuma–
Minto (2004)
Dipel (Btk) Microbial
disruptors
3300 Tabashink et al. (1993)
India Fipronil Phenylpyrazoles 505 Mohan and Gujar (2003)
Cartap Nereistoxin
analogue
24 Perez et al. (2000)
Nicaragua Deltamethrin Pyrethroid 49 800 Perez et al. (2000)
Methamidopho
s
Organophosphate 468 Perez et al. (2000)
Cypermethrin Pyrethroid 232 Perez et al. (2000)
Chlorfluazuron Benzoylureas 200 Perez et al. (2000)
California Permethrin Pyrethroid 206 Shelton et al. (2000)
Spinosad Spinosyns 14.8 Shelton et al. (2000)
Australia Chlorpyrifos Organophosphate 199 Baker and Kovaliski
(1999)
Permethrin Pyrethroid 442 Baker and Kovaliski
(1999)
Florida Fenvalerate Pyrethroid 82 400 Yu and Nguyen (1992)
15
Cyhalothrin Pyrethroid 10 699 Yu and Nguyen (1992)
Carbofuran Carbamate 504 Yu and Nguyen (1992)
Diazinon Organophosphate 73 Yu and Nguyen (1992)
Endosulfan Acyclodiene
organochlorines
25 Yu and Nguyen (1992)
Insecticide resistance in field populations of P. xylostella cause control failures, but
farmers can use insecticides with alternative modes of action to which resistance should
not be present (Verkerk and Wright, 1997). Recurring infestations of P. xylostella and
control failure are also due to natural enemy destruction through the overuse of broad–
spectrum insecticides (Furlong et al., 2004). Early–season spraying of broad–spectrum
insecticides are lethal to parasitoids and thus exacerbate P. xylostella outbreaks
(Grzywacz et al., 2010). Recurring infestations and destruction of natural enemies are of
equal importance in control failure of P. xylostella (Verkerk and Wright, 1997; Talker,
2004). Newer insecticides have been introduced with more selective modes of action,
which are less harmful to natural enemies of P. xylostella (Sayyed and Wright, 2004).
Amongst the insecticides applied in Botswana for control of P. xylostella, primicarb
(carbamate) and Bt insecticides are the least harmful and therefore best for the
conservation of the natural enemies of P. xylostella (Machekano et al., 2017). Spinosad
and pymetrozine are less harmful to biological control agents and are regarded as soft
insecticides. Methomyl (carbamate), organophosphates and pyrethroids are highly toxic
to biological control agents especially Cotesia spp. which are regarded as the most
effective parasitoids in southern Africa (Machekano et al., 2017). Organophosphates,
pyrethroids and carbamates are, however, the most frequently used insecticides for
control of insect pests on vegetables (Obopile et al., 2008; Manyangarirwa et al., 2009;
Nyirenda et al., 2011; Obopile et al., 2013).
The downside is that these insecticides (spinosad and pirimicarb) were introduced in
combination with the older less effective insecticides in spraying programmes resulting in
16
rapid resistance development to newer insecticides (Mazlan and Mumford, 2005; Sayyed
and Wright, 2006). In only two to three years, resistance levels to selected insecticides
can reach major levels for newly introduced insecticides (Zhao et al., 2002; Sayyed and
Wright, 2006; Waters et al., 2009).
No data are currently available on the status of resistance of P. xylostella to registered
commercially available insecticides in southern Africa. The management tactics and
recommendations applied in southern Africa are based on reports from other countries
(Pakistan, Brazil, Australia, China, USA and India) (IRAC, 2015). Insecticide resistance
is based on insect strains with a history of chemical exposure and geographical range of
occurrence (IRAC, 2015). The recommendations from other countries could therefore not
necessarily be applicable to southern Africa. Consequently, the southern African farmers
do not have access to information on P. xylostella resistance for their cropping area. This
lack of information makes control and planning more complicated, and results in farmers
making uninformed decisions influenced by agro–dealers, chemical companies and
advertisements (Nyirenda et al., 2011). The lack of policies on pesticide usage with no
area–wide regulations also complicates integrated resistance management (Ngowi et al.,
2007; Wandaat and Kugbe, 2015). The development of an insecticide resistance
management (IRM) program is imperative to prolong the usage of insecticides and their
efficacy. An IRM program has been implemented in Canada and the USA, which is based
on the IRAC–MoA classification. A similar program was also implemented in Hawaii to
regulate the use of spinosad as constant exposure to insecticides lead to resistance
development (Mau and GusukumaMinuto, 2004). There is, however, no official IRM
program currently available for P. xylostella in South Africa. Examples of resistance to a
number of insecticides in different groups and countries are presented in table 1.3.
Table 1.3: Insecticide class, and country with resistant populations and the mode of action
of the respective classes (Furlong et al., 2013).
Insecticide class Country Mode of action (IRAC,
2012)
Anthranilic
diamides
China (Wang and Wu, 2012) Ryanodine receptor
modulators
17
Avermectins Pakistan (Attique et al., 2006), Brazil (Santos et al.,
2011), Taiwan (Sayyed et al., 2004), China (Zhou et al.,
2011), Malaysia (Iqbal et al., 1996)
Cl– channel activator
Azadirachtin Taiwan (Kao and Cheng, 2001) unknown
Benzoylureas Malaysia (Iqbal et al., 1997), Japan (Morishita, 1998),
Nicaragua (Perez et al., 2000), China (Zhao and Wang),
2006), Brazil (Santos et al., 2011)
Chitin synthesis
inhibitor
Bt (aizawai) USA (Liu et al., 1996), Thailand (Imai and Mori, 1999),
Malaysia (Sayyed et al., 2004), Taiwan (Kao and Cheng,
2001)
Midgut membrane
Bt (Kurstaki) China (Gong et al., 2010), India (Pereira et al., 2006),
USA (Tang et al., 1997), Thailand (Imai and Mori, 1999),
Taiwan (Kao and Cheng, 2001), Malaysia (Sayyed et al.,
2004)
Midgut membranes
Carbamates Taiwan (Kao and Cheng, 2001), South Africa (Sereda et
al., 1997), India (Sannaveerappanavar and Virktamath,
2006), China (Zhou et al., 2011), South Korea (Kim et al.,
2011)
AChe inhibitor
Chlorfenapyr Taiwan (Kao and Cheng, 2001), China (Zhou et al., 2011) Oxidative
phosphorylation
uncoupler
Cyclodiene
organochlorines
India (Lal and Kumar, 2004) ץ–aminobutyric acid
(GABA) Cl– channel
antagonist
Diacylhydrazines China (Zhou et al., 2011) Ecdysone agonist
Indoxacarb Pakistan (Attique et al., 2006), Malaysia (Sayyed et al.,
2006), Australia (Eziah et al., 2009), USA (Zhao et al.,
2006), Brazil (Santos et al., 2011)
Na+ channel blocker
Neonicotinoids Malaysia (Sayyed and Crickmore, 2007)
nAChR antagonists
Nereistoxin analogs India (Mohan and Gujar, 2003), Nicaragua (Perez et al.,
2000), China (Zhou et al., 2011), Taiwan (Kao and
Cheng, 2001)
nAChR blocker
18
Organophosphates Pakistan (Attique et al., 2006), India
(Sannaveerappanavar and Virktamath, 2006), China
(Zhou et al., 2011), Philippines (Sarmiento and Ocampo,
2010), Australia (Eziah et al., 2009), South Africa (Sereda
et al., 1997)
Acetylcholinesterase
(AChe) inhibitor
Phenylpyrazoles Malaysia (Sayyed et al., 2004), India (Mohan and Gujar,
2003), China (Zhou et al., 2011), Taiwan (Kao and
Cheng, 2001).
GABA Cl– channel
antagonist
Pyrethroids Australia (Endersby et al., 2011), China (Endersby et al.,
2011), Brazil (De Oliveira et al., 2011),India (Dhumale et
al., 2009), Japan (Morishita, 1998), Malaysia (Sayyed
and Crickmore, 2007), New Zealand (Cameron et al.,
1997), Philippines (Sarmiento and Ocampo, 2010), South
Korea (Kwon et al., 2009), South Africa (Sereda et al.,
1997), Pakistan (Attique et al., 2006), USA (Shelton et al.,
2000), Nicaragua (Perez et al., 2000).
Na+ channel inhibitor
Spinosyns USA (Baxter et al., 2010), Taiwan (Kao and Cheng,
2001), Malaysia (Sayyed et al., 2004), Pakistan (Attique
et al., 2006).
Nicotinic acetylcholine
receptor (nAChR)
activator
1.9 Resistance mechanisms in Plutella xylostella
Individuals in a population with behavioural resistance developed uncommon behaviour
to survive and reproduce successfully (McGaughey, 1998). For example, P. xylostella
moths oviposit on stems near the soil surface to avoid insecticide applied on leaf surfaces
(Sarfraz et al., 2006). Resistance can also be biochemical (Sarfraz and Keddie, 2005).
Several biochemical mechanisms can be present at the same time and can cause more
than 1000–fold resistance in P. xylostella to insecticides (IRAC, 2018). According to IRAC
(2018), these include the following:
1. Enhanced metabolic detoxification mechanisms:
Microsomal monooxygenases with different forms of cytochrome P450 that play a
major role in P. xylostella resistance to pyrethroids, organophosphates, abamectin
and benzoylphenyl ureas.
Glutathione S–transferases are reported to confer organophosphate resistance.
19
Carboxylesterases are involved in resistance to organophosphates and other
chemical classes of insecticides.
2. Insensitive acetylcholinesterase causes P. xylostella resistance development to
organophosphates and carbamates.
3. Reduced Cry1C binding to the target site in the midgut membrane and reduced
conversion of Cry1C protoxin to toxin are factors in resistance development to the
B.thuringiensis protein Cry1C.
4. Knock–down resistance is caused by a mutation(s) in voltage–gated sodium channels
responsible for pyrethroid resistance.
5. Other mechanisms – include modified GABA–gated chloride channels and reduced
penetration.
1.10 Integrated Pest Management (IPM)
Furlong et al. (2013) published steps for developing and implementing an IPM programme
suitable for most cultivation areas aimed at P. xylostella control. These are:
1. Action thresholds should be calculated for a specific area – a general threshold
cannot be used since each area has its own unique conditions, which change the
dynamics of a P. xylostella population. Action thresholds can reduce the number
of insecticide applications per season.
2. Development of an IRM program using the IRAC–MoA classification scheme is
crucial to ensure long term usage of selected insecticides in spraying programs.
These types of programs can only be successful if growers on a national or
regional level agree and comply.
3. Areas known to be invaded by seasonal migratory populations of P. xylostella can
use warning systems to alert growers of possible infestations. The Canola Council
of Canada (2014) uses a modeling system based on wind trajectory, incorporating
pheromone traps to estimate P. xylostella infestations beforehand.
20
4. Insecticide resistance should be monitored and insecticide applications should be
adjusted when resistance is present. The constant monitoring of resistance is
crucial in preventing control failures with insecticides.
5. Scouts should be trained to effectively and correctly identify pests and to monitor
pest populations and natural enemies.
6. Evaluation of an IPM program is vital to ensure the correct implementation of the
respective methods, which form part of the program. Scouting costs and savings
by reduced insecticide applications should be calculated to ensure economic
viability and delay of resistance evolution.
1.11 Aims and objectives
1.11.1 Aims
The aims of this study were to determine which brassica crops in South Africa can be
used as a trap crop for control of P. xylostella, and to establish the susceptibility of P.
xylostella to selected insecticides in South Africa.
1.11.2 Objectives
The specific objectives of this study were to determine:
the feeding damage and percentage growth of P. xylostella on selected host plants
in no choice tests.
the feeding preference of P. xylostella larvae on selected host plants in two–choice
tests.
the development and oviposition of P. xylostella on selected host plants for
possible use in a Push–Pull strategy.
the susceptibility of P. xylostella to selected insecticides.
The results of this study are presented in the form of chapters with the following titles:
Chapter 2: Cultural control of Plutella xylostella
Chapter 3: Susceptibility of Plutella xylostella populations to selected insecticides
Chapter 4: Conclusion and recommendations
21
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42
Chapter 2: Cultural control of Plutella xylostella
2.1 Abstract
Vegetables are grown in South Arica in rural areas for sustenance. The increase in
cruciferous vegetable production leads to increased Plutella xylostella populations.
Several cases of P. xylostella resistance to insecticides have been reported and prompted
the development of alternative management strategies, with trap crops being the focus of
cultural control. The aim of this study was to determine if any of the five selected P.
xylostella host plant species could be used as trap crops at Pico–Gro. Pico–Gro is a
commercial farm in Glen Austin, Midrand, South Africa. The objectives of this study were
to determine the oviposition and larval feeding preference of P. xylostella in no–choice
and two–choice tests, as well as to determine the larval development time on these
selected host plants. Five known P. xylostella host plant species were selected, viz. pak–
choi (Brassica rapa var. chinensis), cabbage (Brassica oleracea), tatsoi (Brassica
narinosa), kale (Brassica oleracea) and mustard (Brassica juncea). Data were analysed
by means of one–way analyses of variance (ANOVA), meanswere compared by means
of Tukey post–hoc tests. The proportion of P. xylostella that made a choice in the two–
choice tests was calculated, and data were analysed by means of a binomial distribution
test. IBM SPSS ® (version 23, Armonk, NY: IBM Corp). In the two–choice tests,
conducted mustard was preferred for oviposition as well as feeding preference by P.
xylostella larvae. The fact that mustard was the preferred choice over the other crops for
oviposition and feeding preference makes it a viable candidate for a trap crop for P.
xylostella.
Key words: Diamondback moth, feeding preference, oviposition, Plutella xylostella, trap
crops
43
2.2 Introduction
Vegetables in rural areas of South Africa are grown for sustenance (Charleston, 1998).
Generally, small–scale farmers generate a higher income per hectare with vegetables
compared to cereals, root and tuber crops (AVRDC 2006; Mazhawidza and Mvumi,
2017). In the 20 years up to 2012, the global production of cruciferous vegetables
(Brassicaceae) increased by 39% (FAO, 2012). The Brassicaceae consists of 300 genera
and 2 500 to 3 500 species (Marzouka et al., 2010).
Plutella xylostella is a cosmopolitan pest and is globally regarded as the primary pest of
cruciferous vegetables (Furlong et al., 2013). The pest status of P. xylostella, therefore,
increased with the increase in production of cruciferous vegetables. Although P. xylostella
is considered a Brassicaceae specialist (Sarfraz et al., 2010), Furlong et al. (2013) argued
that, with so many species and the global distribution of Brassicaceae, P. xylostella can
be considered a generalist just as much as a specialist. Several cases of P. xylostella
resistance to insecticides have been reported (Talekar and Shelton, 1993; Nyambo and
Löhr, 2005; Ayalew, 2006, Odhiambo et al., 2010, Santos et al., 2011, Zhou et al., 2011;
Agboyi et al., 2013 and Legwaila et al., 2014). This prompted the development of
alternative management techniques, with trap crops the focus of cultural control (Hooks
and Johnson, 2003, Shelton and Badenes–Perez, 2006).
2.2.1 Trap cropping
Trap cropping involves providing a pest with a more attractive host for oviposition and
nutrition than the cultivated crop (Holden et al., 2012). The success of trap crops depends
on the ability of the selected crop to not only attract but also retain pests in numbers
sufficient for the cash crop to experience reduced infestation (Holden et al., 2012).
Insects, in general, depend on host olfactory cues for locating their mates and mating, as
well as finding host plants and oviposition selection (Couty et al., 2006, Silva and Furlong,
2012). Generally, gravid females of P. xylostella are more sensitive to host–derived
volatiles (Mechaber et al., 2002), although there are also exceptions (Martel et al., 2009).
The successful use of a host plant as a trap crop, therefore, depends on specific
behavioural and physiological adaptations in the larval and adult stage. The adult females
44
should find and accept a plant for egg laying and larvae should accept it as well and be
able to develop on it (Bernays and Chapman, 1994). The ultimate trap crop is a dead–
end trap crop, which attracts female moths for oviposition but does not support larval
survival (Shelton and Nault, 2003). Insects have “evolutionary mistakes” when they are
attracted to dead–end trap crops. Insects are attracted to these plants due to their
olfactory restraints but these crops contain lethal underlying components (Badenes–
Perez et al., 2014). Trap cropping has the potential to reduce crop damage while
simultaneously reducing the use of conventional pesticides (Holden et al., 2012).
The choice made by moths to oviposit on certain plant species is essential in the success
of a trap crop since the immature stages of many phytophagous insects, especially
lepidopterans, which are not very mobile (Renwick, 1989). Oviposition by P. xylostella is
affected by stimuli such as leaf surface, abiotic factors and chemosensory stimuli
(Renwick et al., 2006). However, many insects use host plant chemicals in the relevant
concentrations to establish host suitability (Honda, 1995). Insects infesting Cruciferae use
the hydrolysis products from glucosinolates in decision making as stimulants for
oviposition (Hopkins et al., 2009) and larval feeding (Renwick et al., 2006). Variation in
the composition and concentration of glucosinolates can affect host plant suitability for P.
xylostella larvae. Natural selection will, therefore, be in favour of the females that are able
to differentiate between unsuitable and suitable host plants (Li et al., 2000).
Neonate larvae of P. xylostella are immobile and feed on plant material on which they
hatch (Sarfraz et al., 2010). P. xylostella is, therefore, an ideal candidate for trap
cropping. The established trap crops used for P. xylostella are unreliable and it was
reported that growers avoided this cultural practice (Banks and Ekbom, 1999, Shelton
and Badenes–Perez, 2006). Several researchers did, however, continue to study the
development and fitness of this pest on various Brassicaceae (George et al., 2009;
Badenes–Perez et al., 2010; Cunningham, 2012; Nethononda et al., 2016). White
mustard (Sinapis alba) was identified by George et al. (2009) as an effective trap crop for
P. xylostella. Wintercress (Barbarea vulgaris William Townsend Aiton) has also been
found as a preference by P. xylostella moths, but larvae do not survive well on these
plants, which qualifies it as a possible dead–end trap crop (Cunningham, 2012).
45
Although much research has been done on P. xylostella, questions about its host plant
preference in agroecosystems still remain (Newman et al., 2016). Trap cropping is a
viable cultural control method for P. xylostella in growth tunnels, since it has a strong
preference for some Brassicaceae species (Serizawa et al., 2001). Understanding
feeding and oviposition preference can help develop more accurate control measures for
various agroecosystems and assist in the improvement of viable trap crops for control of
P. xylostella in an integrated pest management system, especially in growth tunnels.
2.2.2 Pico–Gro test site
Plutella xylostella is one of the main pests of cruciferous crops cultivated at Pico–Gro in
Glen Austin, Midrand, South Africa (Personal observation). Vegetables and edible flowers
are produced commercially and supplied to both national and international markets. The
set–up consists of 12 greenhouses and an area covered with shade nets (Figure 2.1).
Over 190 plant products are grown at Pico–Gro (Personal observation).
Figure 2.1: Schematic representation of the farm section at Pico–Gro, Glen Austin
Midrand, South Africa.
46
Known host plants of P. xylostella, mustard (Brassica juncea), cabbage (Brassica
oleracea), tatsoi (Brassica narinosa), pak–choi (Brassica rapa var. chinensis) and kale
(Brassica oleracea) are intercropped with various other vegetables in five greenhouses
(Figure 2.3).
The average temperature in these greenhouses was kept at 30 °C and relative humidity
(RH) at 65%. An example of one of these greenhouses is provided in Figure 2.2.
Figure 2.2: Greenhouses used for the production of vegetables and other crops at Pico–
Gro.
Figure 2.3: One of the greenhouses at Pico–Gro where Brassicas are planted. These
greenhouses are divided into bays, each containing plants of a different plant family.
47
The different bays in one of these plant tunnels is depicted in Figure 2.4. It represents a
tunnel were plant species from different plant families are planted together. The plants
are nasturtiums, kale, shiso and bronze fennel.
Figure 2.4: A bay in a tunnel with plants from different families planted.
The arrangement of the various plants to be cultivated per bay in each greenhouse or
shaded area is carefully planned. An example of the layout in three of these greenhouses
is provided in Table 2.1.
48
Table 2.1: Greenhouses and shade net bays with the respective crops planted per bay
in these areas.
Bays Greenhouse 1 Greenhouse 2 Shade
Net
1 Flowers (viola and alyssums) Kale Radish
2 Red vain sorrel and fennel Peas
3 Nasturtiums, kale, shiso and bronze
fennel
Turnip
4 Pak–choi Cabbage
5 Tatsoi Rocket, pak–choi and
tatsoi
6 Rocket Tatsoi and pak–choi
7 Wild rocket
8 Pak–choi and tatsoi
9 Normal and wild rocket
10 Wild rocket
11 Samphire
Pico–Gro supplies national and international markets with various products. Pesticide and
quality requirements are according to the European Union maximum residue levels (EU
MRL) database, which is the standard for worldwide export to be Global Gap registered.
These requirements stipulate that the export product should be insect and residue free.
To ensure adherence, regular tests are done at the airport by the Perishable Product
Export Control Board and Department of Agriculture, Forestry and Fisheries (DAFF) as
well as maximum residue levels testing by the clients (Owner of Pico–Gro).
The implementation of an Integrated Pest Management (IPM) approach consisting of
chemical and cultural control (trap crops), will lower production costs because it can
reduce the number of insecticide applications for control of diamondback moth. It will also
lower the risk of insecticide residue concentrations and the associated health risks.
49
The aim of this study was to determine if any of the five–selected P. xylostella host plant
species, viz. mustard, cabbage, tatsoi pak–choi and kale could be used as trap crops at
Pico–Gro. The objectives of this study were to determine larval feeding and oviposition
preference of P. xylostella in no–choice and two–choice tests, as well as to determine the
larval development time on these selected host plants.
2.3 Material and methods
2.3.1 Plutella xylostella stock colony
Plutella xylostella larvae were collected from cabbage at a commercial farm in Glen
Austin, Midrand. The infested plant material was kept in plastic containers (40 x 20 x 15
cm) with aerated sides. Moths were transferred from these containers to wooden screen
cages (0.75 m (w) x 1 m (h)) with potted cabbage plants for oviposition. Eggs were
collected daily and kept in small plastic containers (52 mm high, 30 mm in diameter) with
a steel mesh–infused lid, in a rearing room at 26 ± 1 ºC, 65 ± 5% humidity and 14L:10D
photoperiod. Once emerged from the eggs, larvae were transferred into plastic containers
similar to the ones described above and reared on cabbage in a laboratory at 25 ±1 ºC.
2.3.2 Larval feeding preference for selected Brassicas
Mustard, cabbage, tatsoi, pak–choi and kale were planted in pots under shade nets at the
North–West University, Potchefstroom (Figure 2.5). For larval choice experiments, leaves
from five–weeks–old plants were used.
50
Figure 2.5: Brassica plants in pots that were used in no–choice and two–choice tests.
a: mustard, b: cabbage, c: tatsoi d: pak–choi and e: kale.
2.3.3 Larval feeding choice tests
2.3.3.1 No–choice tests
Leaf disks (3 cm diameter) were punched from mustard, cabbage, tatsoi, pak–choi and
kale. The bottoms of Petri dishes (100mm (d) x 15mm (h)) were covered with a 3 mm
layer of agar–agar (which contained no nutrients) to prevent desiccation of the plant
material. A single disc of plant material from a plant species was placed in the centre of
a Petri dish. The mass of 10 P. xylostella larvae (3rd instar) was determined before being
placed individually onto the agar next to the side of the Petri dish. The Petri dishes were
kept in a rearing room at 26 ±1 ºC, 65 ± 5% humidity and 14L: 10D photoperiod. Larvae
were weighed again after 48 hours to determine the mean mass gain of larvae per plant
species. This was done as an indication of the suitability of the respective host plant
species for larval growth. Each leaf disk was scanned after 48 hours with a Samsung S9+
cell phone, picture size (4:3 12MP) for foliar analysis application with BioLeaf
(http://bioleaftech.co.za/) (Machado et al., 2016), after which the percentage leaf surface
consumed was calculated (Figure 2.6). The no–choice test with each plant species
consisted of 10 replicates with five larvae used per replicate.
51
Figure 2.6: Calculation of the percentage damaged (defoliation) leaf area using the
BioLeaf application. The damaged area is shown in red and calculated as percentage
‘defoliation’.
2.3.3.2 Two–choice tests
To determine larval feeding preference for the respective plant species, two–choice tests
were done by placing a single leaf disc (each 3 cm in diameter) from two different host
plants, 4 cm apart and 5 cm away from the side per Petri dish. The same host plants used
in the no–choice tests were pair–wise presented. The bottoms of Petri dishes were
covered with agar–agar as described above (see 2.1). Five larvae were placed in the
centre of the Petri dish at an equal distance away from the respective leaf discs. Feeding
preference of the larvae was recorded and feeding damage was calculated after 48 hours
as described in 2.1. There were 10 replicates with five larvae for each combination.
52
2.3.4 Oviposition preference tests
Oviposition preference of P. xylostella moths was determined in two–choice tests with the
same plant combinations used in the two–choice larval preference tests (see 2.2). The
sex of 3rd and 4th instar larvae was determined according to the characteristics described
by Liu and Tabashnik (1997). The 5th abdominal segment of male larvae is lighter in colour
compared to that of female larvae where all segments are the same colour (Figure 2.7).
These larvae were kept individually in small plastic containers (20 cm x 15 cm x 7 cm)
until pupation.
Figure 2.7: Distinguishing characteristics of male and female Plutella xylostella larvae.
The male larvae have a lighter coloured 5th abdominal segment than female larvae.
On the day of exclusion, one male– and one female moth were released into containers
(40 cm x 20 cm x 15 cm) with ventilation openings on two opposite sides. From the
selected plant species, two were selected for each oviposition test with 20 replicates for
each two–choice oviposition test. The plants were placed approximately 20 cm apart and
watered daily. The plants were removed and carefully taken apart, 48 hours after moths
were released into the cages. Eggs on the selected plant pieces were counted under a
stereomicroscope (Nikon SMZ 1500).
2.3.5 Development time
Pupae were collected from the rearing colony and placed into containers (40 cm x 20 cm
x 15 cm) with ventilation openings on two opposite sides. Host plant species, viz. mustard,
cabbage, tatsoi, pak–choi and kale were presented in all possible combinations in these
containers (two plants per container). The plants were kept in each container for 24 hours
before being removed and transferred to similar containers, but without moths. Therefore,
Female
Male
53
the emerging moths were immediately exposed to the test plant combination, without any
previous experience of other host plants. The oviposition containers as well as the plants
removed from the oviposition containers that were transferred to insect–free containers,
were kept at 26 ±1 0C, 65 ± 5% humidity and 14L: 10D. Total development time (days)
from 10 eggs to moth emergence on each of the selected crops were recorded with 10
replications.
2.3.6 Data Analysis
Data were analysed for normality and homogeneity before further analyses. One–way
analysis of variance (ANOVA) was used and means were compared with a Tukey post–
hoc test if the data was normally divided and homogeneous. IBM SPSS ® (version 23,
Armonk, NY: IBM Corp) was used for statistical analyses and graphical representation.
The proportion of P. xylostella larvae that made a choice in the two–choice oviposition
and feeding tests was calculated, and data was analysed by means of a binomial
distribution test IBM SPSS ® (version 23, Armonk, NY: IBM Corp) was used for statistical
analyses and graphical representation. Significance between selected combination was
established by mean of t–tests and displayed as *P<0.05, **P<0.01 and ***P<0.001.
2.4 Results
Choice tests
2.4.1. No–choice tests
The mean mass increase by larvae that fed on the respective host plant species differed
significantly (F4, 20 = 11,48; P<0.001). Larvae that fed on mustard gained significantly less
mass than larvae that fed on pak–choi and tatsoi, but their mass gained did not differ
significantly from cabbage and kale–fed larvae. The increase in the mean larval mass of
P. xylostella larvae that fed on pak–choi was the highest, but it did not differ from larval
mass gained on tatsoi (Figure 2.8).
54
Figure 2.8: Increase in mean larval mass (g) after 48 hours of feeding on host plant
species, viz. cabbage, kale, mustard, pak–choi, tatsoi in no–choice tests. Bars capped
with the same letter are not significantly different (P < 0.05).
An example of feeding damage by P. xylostella larvae to a leaf disk of the respective host
plants evaluated in no–choice experiments is shown in figure 2.9.
F4, 20
= 11,48; P<0.05
ab
ab
a
c
bc
Ma
ss in
cre
ase
(m
g)
± S
E
Crops
55
Figure 2.9: Leaf disks showing Plutella xylostella feeding damage in the no–choice
experiments; a: mustard, b: cabbage, c: pak–choi, d: tatsoi and e: kale.
The mean percentage P. xylostella damage differed significantly between cabbage, kale,
mustard, pak–choi and tatsoi leaf disks (F4, 20 = 87,11; P<0.001). The mean percentage
damage inflicted by P. xylostella larvae was significantly higher on mustard compared to
cabbage, kale, tatsoi and pak–choi. However, significantly more pak–choi leaf material
was consumed by P. xylostella larvae compared to cabbage, kale and tatsoi. There was,
however, no significant difference in percentage damage caused by larval feeding on
cabbage, kale and tatsoi (Figure 2.10).
a c b
d e
56
Figure 2.10: Mean percentage damage after 48 hours of feeding on the respective host
plant species, viz. cabbage, kale, mustard, pak–choi, tatsoi in no–choice tests. Bars
capped with the same letter are not significantly different (P < 0.05).
2.4.2 Two–choice tests
The feeding preference of P. xylostella larvae in two–choice tests was significantly higher
on pak–choi, mustard and tatsoi compared to kale and cabbage (Figure 2.11).
F4, 20
= 87,11; P<0.05
c
b
a
a
a
57
Figure 2.11: Preference of Plutella xylostella larvae for different host plant species in
two–choice tests after 48 hours. Significance indicated by **P<0.01 and ***P<0.001. ‘NC’
indicates the number of larvae (out of 50 per combination) that did not make a choice.
2.4.2.1 Percentage damage
The differences in the quantity of leaf material removed by feeding larvae from leaf disks
from the respective host plant species in the two choice tests are shown in figure 2.12.
-1, -0,8 -0,6 -0,4 -0,2 0, 0,2 0,4 0,6 0,8 1,
Cabbage x Pak-choi
Cabbage x Tatsoi
Cabbage x Mustard
Cabbage x Kale
Tatsoi x Pak-choi
Kale x Pak-choi
Kale x Tatsoi
Mustard x Tatsoi
Mustard x Kale
Mustard x Pak-choi
Preference proportion
Ho
st-
pla
nt
co
mb
ina
tio
ns
Plant 1 Plant 2
NC 5
NC 14
***
***
**
***
***
***
***
***
**
***
58
Figure 2.12: Leaf disks provided in the two–choice test showing Plutella xylostella
feeding damage: a: cabbage vs pak–choi, b: cabbage vs mustard, c: kale vs mustard, d:
cabbage vs pak–choi, e: kale vs pak–choi, f: kale vs cabbage, g: mustard vs pak–choi,
h: mustard vs tatsoi, i: pak–choi vs tatsoi and j: kale vs tatsoi.
2.4.2.2 Mean percentage damage
The mean percentage damage of P. xylostella larvae that fed on mustard, pak–choi and
tatsoi was significantly higher when compared to the damage inflicted by larvae that fed
a
d
c
b
e
g
f
h
59
on cabbage and kale. There was, however, no significant difference in percentage
damage between pak–choi, tatsoi and mustard. The mean defoliation from larvae that fed
on cabbage and kale did also not differ significantly (Figure 2.13).
Figure 2.13: Mean percentage damage after 48 hours of feeding on the respective host
plant species, viz. cabbage, kale, mustard, pak–choi, tatsoi in no–choice tests. Bars
capped with the same letter are not significantly different (P < 0.05).
2.4.2.3 Oviposition preference
The mean number of eggs laid by P. xylostella in two–choice tests differed significantly.
Significantly higher numbers of eggs were laid on mustard, pak–choi and tatsoi when
compared to kale and cabbage (Figure 2.14).
a
bc
a
c
c
F8, 40
= 42; 12 P<0.05
60
Figure 2.14: The preference of Plutella xylostella moths for different host–plant species
in oviposition tests after 48 hours. Significance indicated by ***P<0.001.
2.5 Discussion
No–choice tests where P. xylostella are only exposed to one host plant are used to
determine specific development characteristics such as growth to compare between
various host plants (De Bortoli et al., 2013). Newman et al. (2016), however, used multiple
plant species within the Brassicaceae Brassicaceae plant family to establish larval
ingestion rates as well as contact preference. The tests were used to assess alternate
host plants for use as a trap crop. The study by Newman et al. (2016) showed that larval
growth was unfavourable on high–preferred oviposition species potentially having
negative effects on neonate larvae concluding the possible use of black mustard as a trap
crop. Niu et al. (2014) studied the reproductive potential, survival, and development of P.
xylostella on eight cruciferous species, i.e. Descurainia sophia (L.), Cardamine hirsuta
L., Capsella bursa–pastoris (L.), Thlaspi arvense L., Rorippa indica (L.), Orychophragmus
violaceus (L.), Cardamine leucantha (Tausch) and Cardamine macrophylla. The
development of P. xylostella differed greatly between plant species according to Niu et al.
-1 -0,8 -0,6 -0,4 -0,2 0 0,2 0,4 0,6
MustardxPak-choi
Pak-choixKale
MustardxTatsoi
MustardxKale
CabbagexKale
TatsoixKale
TatsoixCabbage
MustardxCabbage
TatsoixPak-choi
Pak-choixCabbage
Oviposition proportion
Sele
cte
d c
om
bin
ation
Plant 1 Plant 2
***
***
***
***
***
***
***
***
***
***
61
(2014). The study by Niu et al. (2014) established that certain plant species such as C.
macrophylla had the longest development time, lighter weight per pupae and high
oviposition preference all good characteristics for a trap crop used for P. xylostella control.
No–choice tests gave valuable information regarding monoculture–cropping areas,
however, two–choice and development tests are essential to better understand host
preference of P. xylostella. Growing tunnels with various host plants or environments with
bordering wild plants in a nursery setting as seen at Pico–Gro is the ideal area to establish
known host plants as trap crops.
De–Bortoli et al. (2013) have performed multi–choice preference tests with cauliflower,
broccoli, cabbage and collard greens. Plutella xylostella larvae favoured collard greens,
however, cauliflower was preferred for oviposition by adult females (De Bortoli et al.,
2013). In the two–choice tests conducted mustard was preferred for oviposition as well
as feeding preference by P. xylostella larvae. The fact that mustard was the preferred
choice over the other crops for oviposition and feeding preference makes it a viable
candidate for a trap crop for P. xylostella. Charleston and Kfir (2000) reported the similar
results on a different cultivar with P. xylostella females to prefer Brassica juncea juncea
(Indian mustard) for oviposition compared to commonly grown crops such as cauliflower,
broccoli and Chinese cabbage. It therefore showed promise as a trap crop for P. xylostella
(Charleston and Kfir, 2000). The similar results are seen above for Brassica juncea var.
integrifolia (Giant red mustard) as it is preferred for oviposition compared to kale,
cabbage, tatsoi and pak–choi.
Plutella xylostella develops faster and survive better on Brassica napus and Brassica
compestris when compared to Brassica rapa, Brassica oleracea botrytis and Raphanus
sativus (Saeed et al., 2010). The similar results were found on different crop species
where P. xylostella developed faster on mustard than compared to cabbage, kale, pak–
choi and tatsoi. Oviposition was preferred on garden cress (Lepidium sativum) (L.) with
wintercress (Barbarea vulgaris) (L.) and black mustard (Brassica nigra) (L.) following
closely behind (Newman et al., 2016). The ingestion rates of the various plants with the
highest on aubretia (Aubretia deltoidea) (L.) and the lowest on black mustard (Newman
et al., 2016). In the study by Newman et al. (2016) black mustard was highly preferred for
62
oviposition, however, the ingestion rates were the lowest for the same crop. Mustard was
also highly preferred for oviposition when compared to pak–choi, tatsoi, kale and cabbage
but have contradicting results with the feeding preference (ingestion rate) concluding to
be the highest of the selected crop species.
Niu et al. (2014) established that development from egg to adult had significant variance
and was longer on R. indica (15.8 d) and C. macrophylla (20.8 d). The same results were
observed with mustard (10.6 d) and kale (16.9 d), however, the development time was
faster for the selected crops than the crops used in the study by Niu et al. (2014). Larval
development time of P. xylostella on cabbage was shorter than on kale and pak–choi.
When comparing this result with the two–choice and oviposition results it would make
sense that cabbage and kale had longer development times as they resulted in the lowest
feeding and oviposition preference and defoliation percentage. The presence of pak–choi
as one of the crops on which P. xylostella development is quicker is not surprising with
pak–choi present in all the highest subsets in feeding and oviposition preference and
defoliation percentage. Weight gained by P. xylostella larvae that fed on leaf tissue in no–
choice tests were the lowest for larvae feeding on mustard in comparison with the other
selected crops. Niu et al. (2014) had similar results on other crop species, however
instead of weighing larvae, pupae were weighed with T. arvense having the lightest pupae
(Niu et al., 2014). Oviposition on C. macrophylla, O. violaceus and Ca. bursa–pastoris
compared to R. indica indicated a fecundity of 305–351 eggs/female and 134 eggs/female
irrespectively (Niu et al., 2014). Oviposition on mustard and kale showed significant
variance with 16–27 eggs/female and 2–4 eggs/female irrespectively.
Choice attest and larval development evaluations conducted indicate the use of Brassica
juncea var. integrifolia (Giant red mustard) as a viable trap crop for the control of P.
xylostella. The integration of mustard as a trap crop can be used at sites like Pico–Gro to
help control P. xylostella populations. Planting the trap crop (mustard) in between
selected crops (tatsoi, pak–choi, kale and cabbage) can reduce the number of individuals
in the population by removing the trap crop after infestation occurs. The continued
planting of trap crops like mustard and removing infested trap crop plants may reduce the
population below the economic injury level.
63
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69
Chapter 3: Susceptibility of Plutella xylostella populations
to selected insecticides
3.1 Abstract
Plutella xylostella is the most important insect pest of Brassica crops worldwide and
occurs wherever its host plants are cultivated. Insecticide application is the main control
strategy and concerns are raised about the susceptibility of P. xylostella to insecticides in
South Africa. Plutella xylostella populations were sampled from two localities, Nelspruit
(Mpumalanga province) and Bapsfontein (Gauteng province). The toxicity of three
insecticides used for control of P. xylostella in South Africa, viz. lambda–cyhalothrin,
flubendiamide and spinosad has been estimated for both these populations using an
IRAC approved bioassay method. In the absence of a reference population, comparisons
with the recommended label rates were performed. When comparing the susceptibility of
the two populations (Nelspruit (N2018–01) and Bapsfontein (B2018–01)) for lambda–
cyhalothrin the LC80 values are higher (N2018–01: 9.35 and B2018–01: 24.87) than the
recommended dosage of 8ppm). These populations are highly susceptible to
flubendiamide with LC80 values of 2.70 (B2018–01) and 2.24 (N2018–01) 0% compared
to the recommended dosage of 48ppm and to spinosad with LC80 values of 24.87ppm
(B2018–01) and 9.35 (N2018–01) compared to the recommended dosage of 216ppm.
Plutella xylostella remains a persistent and extensive pest of Brassicaceae. Resistance
development to insecticides is a reality. It is costly to control the pest, but in South Africa
(Nelspruit and Bapsfontein), P. xylostella is still highly susceptible to two active
ingredients (flubendiamide and spinosad) which is important for effective control of P.
xylostella populations.
Keywords: Plutella xylostella, spinosad, lambda–cyhalothrin, flubendiamide, South
Africa, susceptibility
70
3.2 Introduction
Plutella xylostella is the most important insect pest of Brassica crops worldwide and it
occurs wherever its host plants are cultivated (Talekar and Shelton, 1993). For decades
P. xylostella was not an economically important pest in South Africa and insecticides
provided effective control on various crops (Dennill and Pretorius, 1995). Outbreaks of P.
xylostella in South Africa occurred in the early 1990s (Dennill and Pretorius, 1995). Since
then, insecticide application became the main control strategy and concerns are raised
about the susceptibility of P. xylostella to insecticides in South Africa (Sereda et al., 1997).
Various local populations of P. xylostella were found to be less susceptible to frequently
used insecticides (Sereda et al., 1997). These populations became so severe that farmers
sprayed their fields more frequently than recommended to overcome this problem (Dennill
and Pretorius, 1995; Sereda et al., 1997). Increased damage levels were reported on
crops in regions where insecticides were applied frequently (Waladde et al., 2001). High
levels of parasitism of P. xylostella were, however, reported in unsprayed crops in
Gauteng, North–West and Eastern Cape provinces of South Africa (Smith and Villet,
2002). The use, overuse and exploitation of broad–spectrum insecticides in some areas
could possibly have eradicated the natural enemies of P. xylostella in these areas (Sereda
et al., 1997). Dennill and Pretorius (1995) sampled only one parasitoid in a cabbage field
in Pretoria where insecticides were applied regularly. In the same year and area, Kfir
(1997) sampled and documented 21 species of parasitoids in areas where no insecticides
were applied.
It was mentioned that in Togo and Benin (Countries in West Africa) farmers use
insecticides in high dosages with frequent applications (Agboyi et al., 2016). However,
prior to the study done by Machekano et al. (2019), no comprehensive study was done
on practices, perceptions and knowledge in Botswana and southern Africa to better
understand the overuse of pesticides. The misuse of pesticides and the differences in
manufacturer recommendations and realities can all be linked to a lack of research
(Machekano et al., 2019).
71
3.2.1 Insecticide resistance
Yamada and Koshihara (1978) listed conditions contributing to the development of
resistance to insecticides by P. xylostella. These include long cultivation seasons,
monoculture cultivation of Brassicaceae and high temperatures. Plutella xylostella
infestations are severe in countries with warm climates since the pest completes multiple
generations per year (Liu et al., 1981).
Constant cultivation of host crops and the short life cycle of P. xylostella contributes to
the continuous development and population increase of the pest that resulted in 25
generations being sprayed with synthetic insecticides each year causing the development
of resistance to various insecticides in Malaysia (Sayyed et al., 2004). Farmers in
Zimbabwe and Kenya also depend on synthetic insecticides (pyrethroids,
organophosphates and carbamates) (Oruku and Ndun'gu, 2001; Sithole, 2005). Due to
their lack of knowledge on resistance and newly developed insecticide groups, poor
farmers in Africa and Asia (Rauf et al., 2004) aggravate resistance development to
insecticides. These farmers rely on broad–spectrum insecticides already overused and
more toxic to natural control agents (Badenes–Perez and Shelton, 2006). With no insect
resistance management (IRM) strategy in place, the pattern of introducing new
insecticides and failure of these insecticides to control P. xylostella populations is
continuing (Wright, 2004; Mau and Gusukuma–Minuto, 2004; Santos et al., 2011; Kang
et al., 2017).
The status of P. xylostella as one of the most damaging lepidopteran pests worldwide
could be ascribed to its ability to develop resistance to all conventional insecticide classes
in the field (Liu et al., 2015). With the introduction of newer insecticides (spinosad,
avermectin, fipronil and indoxacarb), different modes of action entered the market.
Resistance development is, however, enhanced with these insecticides not being rotated
(Amit et al., 2004). Resistance to spinosad was recorded in field populations of P.
xylostella in the United States (Zhao et al., 2002) and Malaysia (Sayyed et al., 2004),
while resistance to indoxacarb was reported from Pakistan (Attique et al., 2006).
Emamectin benzoate is a second generation semi–synthetic avermectin insecticide
72
(Syngenta, 2004), but cases of resistance to avermectins were reported in China (Liang
et al., 2003) and Malaysia (Sayyed et al., 2004).
The development of insecticide resistance is a global problem and it is critical for crop
protection and resistance management to clarify the mechanisms that establish
resistance (Xia et al., 2018). According to Liu et al. (2015) the first commercial insecticide
belonging to the diamide group is chlorantraniliprole. The diamide group of insecticides
became commercially available in 2006 with flubendiamide derived from
benzenedicarboxamide shortly followed by cyantraniliprole and chlorantraniliprole from
the anthranilic diamides (Nauen and Steinbach, 2016). This insecticide group is active on
the insect ryanodine receptors in the endoplasmic reticulum (Nauen and Staeinbach,
2016). In 2013, more than $1.2 billion of diamides were sold globally (Nauen and
Staeinbach, 2016). After only 52 generations of selection, P. xylostella showed resistance
to chlorantraniliprole in China (Liu et al., 2015).
The recurring selection pressure imposed onto P. xylostella by the application of
insecticides in a Brassica cultivation area in Brazil, caused multiple insecticide resistance
(Neto et al., 2016). Plutella xylostella has developed resistance to spinosad and
chlorfenapyr, but there is no shift in the resistance levels of chlorantraniliprole in field
populations (Neto et al., 2016). Cross–resistance between chlorfenapyr and spinosyns
was not found, however cross–resistance was found between spinetoram and spinosad
(Neto et al., 2016).
3.2.2 Research and case studies
Research on the management of P. xylostella in SA is limited with minimal data available
compared to other countries (Gryzwacz et al., 2010) (Figure 3.1). The efficacy of control
by a pyrethroid (cypermethrin) and Bt (B. thuringiensis var. kustaki) to P. xylostella was
evaluated in Botswana (Legwaila et al., 2014, Legwaila et al., 2015). There is, however,
no information available on the current susceptibility of P. xylostella to insecticides
registered for control in South Africa.
73
Figure 3.1: The number of P. xylostella insecticide resistance reports from countries in
the world (IRAC, 2018).
Insecticides for control of P. xylostella is registered in 14 groups with more than 160
active ingredients worldwide (Table 3.1). This multitude of registrations indicates the
difficulty of maintaining a high susceptibility of P. xylostella for insecticides.
110
13 10 10 8
24
14
1 0 0 0 0 0 2
0
20
40
60
80
100
120
NO
OF
RES
ISTA
NC
E R
EPO
RTS
(A
RTI
CLE
S)
COUNTRIES
74
Table 3.1: Insecticide groups registered for control of P. xylostella worldwide with examples of active ingredients (IRAC, 2018).
Insecticide group
Group number
Active ingredients
Diamides 28 Chlorantraniliprole, Cyantraniliprole, Flubendiamide
Carbamate 1A Alanycarb, Aldicarb, Bendiocarb, Benfuracarb, Butocarboxim, Butoxycarboxim, Carbaryl, Carbofuran, Carbosulfan, Ethiofencarb, Fenobucarb, Formetanate, Furathiocarb, Isoprocarb, Methiocarb, Methomyl, Metolcarb, Oxamyl, Pirimicarb, Propoxur, Thiodicarb, Thiofanox, Triazamate, Trimethacarb, XMC, Xylylcarb
Organophosphate 1B Acephate, Azamethiphos, Azinphos–ethyl, Azinphos–methyl, Cadusafos, Chlorethoxyfos, Chlorfenvinphos, Chlormephos, Chlorpyrifos, Chlorpyrifos–methyl, Coumaphos, Cyanophos, Demeton–S–methyl, Diazinon, Dichlorvos/ DDVP, Dicrotophos, Dimethoate, Dimethylvinphos, Disulfoton, EPN, Ethion, Ethoprophos, Famphur, Fenamiphos, Fenitrothion, Fenthion, Fosthiazate, Heptenophos, Isofenphos, Isoxathion, Malathion, Mecarbam, Methamidophos, Methidathion, Mevinphos, Monocrotophos, Naled, Omethoate, Oxydemeton–methyl, Parathion, Parathion–methyl, Phenthoate, Phosalone, Phorate, Phosmet, Phosphamidon, Phoxim, Profenofos, Propetamphos, Prothiofos, Pyraclofos, Pyridaphenthion, Quinalphos, Sulfotep, Tebupirimfos, Temephos, Terbufos, Tetrachlorvinphos, Thiometon, Triazophos, Trichlorfon, Vamidothion, Pirimiphos–methyl, Imicyafos, Isopropyl O–(methoxyaminothio–phosphoryl) salicylate
Cyclodiene organochlorines
2A Chlordane, Endosulfan
Fiproles 2B Ethiprole, Fipronil
Pyrethroids 3A Acrinathrin, Allethrin, d–cis–trans Allethrin, d–trans Allethrin, Bifenthrin, Bioallethrin, Bioallethrin S–cyclopentenyl, Bioresmethrin, Cycloprothrin, Cyfluthrin, beta–Cyfluthrin, Cyhalothrin, lambda–Cyhalothrin, gamma–Cyhalothrin, Cypermethrin, alpha–Cypermethrin, beta–Cypermethrin, theta–Cypermethrin, zeta–Cypermethrin, Cyphenothrin [(1R)–trans– isomers], Deltamethrin, Empenthrin [(EZ)– (1R)– isomers], Esfenvalerate, Etofenprox, Fenpropathrin, Fenvalerate, Flucythrinate, Flumethrin, tau–Fluvalinate, Kadathrin, Pyrethrins (pyrethrum), Halfenprox, Phenothrin [(1R)–trans– isomer], Prallethrin, Resmethrin, Silafluofen, Tefluthrin, Tetramethrin, Tetramethrin [(1R)– isomers], Tralomethrin, Transfluthrin, Permethrin
Spinosyns 5 Spinetoram, Spinosad
Avermectin 6 Abamectin, Emamectin benzoate, Lepimectin, Milbemectin
Benzylureas 15 Bistrifluron, Chlorfluazuron, Diflubenzuron, Flucycloxuron, Flufenoxuron, Hexaflumuron, Lufenuron, Novaluron, Noviflumuron, Teflubenzuron, Triflumuron
Dicylhyydrazine 18 Chromafenozide, Halofenozide, Methoxyfenozide, Tebufenozide
Oxadiazines 22A Indoxacarb
Semicarbazones 22B Metaflumizone
Pyridalyl UN
Chlorfenapyr 13 Chlopenapyr
Bt 11 Florbac, Dipel
75
The aim of this study was to evaluate the susceptibility of P. xylostella populations from
two areas in South Africa, namely Nelspruit (Mpumalanga province) and Bapsfontein
(Gauteng province) to selected insecticides with different modes of action.
3.3 Material and methods
3.3.1 Plutella xylostella sampling
In 2018, large numbers of P. xylostella larvae were collected on canola at Nelspruit
(25°26'14.2”S; 30°59'34.6”E) and on cabbage in Bapsfontein (26°94'34.2”S;
28°52'96.4”E) and used to establish rearing colonies. More than 500 larvae were
collected from each locality. An identification code was assigned to each collected
population and used for reference thereafter, viz. Bapsfontein (B2018–01) and Nelspruit
(N2018–01). The larvae were transported to the laboratory immediately after collection,
they were provided with additional food to limit possible temperature and humidity stress
and to ensure that they had enough food available at all times.
3.3.2 Experimental design
Commercial formulations of spinosad (spinosyn), lambda–cyhalothrin (pyrethroid) and
flubendiamide (diamide) were used in leaf–dip bioassays. Field collected larvae (F0) were
used for the initial range finder bioassays of spinosad, lambda–cyhalothrin and
flubendiamide for both P. xylostella populations prior to the toxicological tests. The
remainder of the F0 larvae was used to establish the respective rearing colonies. Plutella
xylostella larvae were kept in plastic containers (40 x 20 x 15 cm) with aerated sides.
Moths were transferred from these containers to wooden screen cages (0.75 m (w) x 1 m
(h)) with potted cabbage plants for oviposition. Eggs were collected daily and kept in small
plastic containers (52 mm high, 30 mm in diameter) with steel mesh–infused lids, in a
rearing room at 26 ± 1 ºC, 65 ± 5% humidity and 14L:10D photoperiod. Once emerged
from the eggs, larvae were transferred into plastic containers similar to these described
above and reared on cabbage in a laboratory at 25 ±1 ºC.
The susceptibility of the two P. xylostella populations to selected insecticides was
estimated using the IRAC Susceptibility Test Method 018.
76
Three stock solutions were prepared for each insecticide tested (replicates). Eight
accurate dilutions (concentrations) were prepared from each stock solution and 0.2 gL–1
Triton X added as a wetter (Figure 3.2). The control treatment consisted of water and
Triton X (0.2 gL–1).
Figure 3.2: Dilutions of the insecticides with a wetting agent added (Triton X).
Brassica oleracea (cabbage) leaves were sampled from plants planted in pots. These
leaves were cut into smaller pieces, (±5 x 2.5 cm). For the bioassays, 32 well trays
(Frontier: scientific services) were used. The leaf pieces (24 per concentration) were
individually dipped in the insecticide concentrations for 10 seconds and placed on a drying
rack (Figure 3.3).
Figure 3.3: Leaves left to dry off before inoculation.
77
After the leaf pieces were dry, they were transferred to bioassay trays labeled with the
corresponding concentration. The bottom of each well in these trays was covered with
a thin layer of agar–agar to prevent leaf pieces from desiccation. One 3rd instar P.
xylostella larva was placed on the leaf piece per well. The trays were sealed with
transparent, ventilated lids (Figure 3.4).
Figure 3.4: Containers with a single Plutella xylostella larva on one leaf piece per well
placed on agar–agar and sealed with transparent, ventilated lids.
All treatment trays were kept in an incubator at 25 ± 1°C and a 14:10 L:D photoperiod.
Mortality was assessed after 72 hours for lambda–cyhalothrin and spinosad. The
assessment period for flubendiamide was after 96 hours.
3.3.3 Data Analysis
Data on P. xylostella larval mortality was subjected to probit analysis using PoloSuite®
software (version 1.8) (LeOra Software).
The software provides the slope, lethal concentrations (LC’s) and 95% fiducial limits (FL)
of the lethal concentrations (LC’s) and tests the dose–mortality response for linearity.
Mortality was corrected for control mortality by means of Abbott’s formula (Abbott, 1925).
The estimated LC80 and LC95 values were compared with the maximum recommended
field rate. The assessment of potential insecticide control failure was carried out using the
78
same experimental unit as described for the concentration–response bioassay, but
comparing this mortality caused by the recommended label rate of each insecticide (mid–
concentration from the registered range) and the lower threshold at LC80 estimated for
each compound (Silva et al., 2011). The 80% mortality was used as a reference because
this is the minimum level of efficacy required for registration of an insecticidal compound.
This is the minimum level of efficacy without control failure due to insecticide resistance.
The insect mortality caused by the label rate was considered to be significantly lower than
80% when the recommended rate was lower than the lower threshold of 95% fiducial
interval of the LC80 of the insecticide for the tested insect population (Silva et al., 2011).
The registered and recommended label rates of the three insecticides in South Africa are:
8 ppm for lambda–cyhalothrin (mid–dosage), 48 ppm for flubendiamide and 144 ppm for
spinosad on cabbage for P. xylostella.
3.4 Results
The probit analyses results of spinosad (spinosyn), lambda–cyhalothrin (pyrethroid) and
flubendiamide (diamide) tested for both P. xylostella populations (B2018–01 and N2018–
01) are presented in table 3.2. The responses fitted the log (dose)/probit (mortality) model.
3.4.1 Spinosad
The slope of the response line to spinosad from N2018–01 was higher compared to that
of B2018–01, resulting in a lower LC50 value for N2018–01 compared to B2018–01 (Table
2.2). The recommended label rate (144 ppm) was higher than the LC95 and application at
the recommended rate will therefore result in 100% mortality based on the estimates of
the probit model (Table 3.2). The recommended rate is 24 times higher than the LC95.
3.4.2 Lambda–cyhalothrin
The slopes of the response lines of the two populations to lambda–cyhalothrin ranged
from 1.45 (B2018–01) to 3.68 (N2018–01) and the LC50 from 5.53 to 6.55 for N2018–01
and B2018–01, respectively. The LC50, LC80 and LC95 for both populations were higher
than the recommended dosage of 4 ppm (Table 3.2), indicating possible control failure
for both populations by this insecticide.
79
3.4.3 Flubendiamide
The slope of the response line to flubendiamide from N2018–01 was 1.86 and for B2018–
01, 0.82. The two populations (N2018–01 and B2018–01) susceptibility to flubendiamide
indicated that the LC50 values do not differ significantly (P > 0.05): N2018–01 (0.79) and
B2018–01 (0.25) (Table 3.2). The slope of N2018–01 was 1.86 (SE = 0.17) and (SE =
0.09). The recommended label rate (48 ppm) was almost eight times higher than the LC95
for both populations and would therefore result in 100% mortality based on the estimation
of the probit model (Table 3.2)
80
Table 3.2: Log dose probit mortality for P. xylostella populations from Nelspruit (N2018–01) and Bapsfontein (B2018–01).
Active ingredient
Recommended dosage (ppm)
Population n LC50 FL 95% LC80 FL 95% LC95 (ppm)
χ2 df H Slope SE
Spinosad 216 B2018–01 360 0.61 0.45–
0.88 1.95 1.23–5.07 5.93 2.8 3 0.9 1.66 0.22
N2018–01 288 0.47 0.31–
0.84 1.09 0.66–4.22 2.41 2.5 2 1.0 2.32 0.26
Lambda–
cyhalothrin 8
B2018–01 360 6.55 5.67–
7.79 24.87 18.98–35.02 88.92 0.2 3 0.08 1.45 0.21
N2018–01 360 5.52 3.86.89 9.35 7.51–13.04 15.46 5.8 4 1 3.68 0.37
Flubendiamide 48 B2018–01 432 0.25 0.16–
0.38 2.70 1.65–5.51 25.92 2.4 4 0.6 0.82 0.09
N2018–01 360 0.79
0.59–
1.04 2.24 1.64–3.47 6.03 2.3 3 0.8 1.86 0.17
n = number of larvae tested; FL = fiducial limits; LC50, LC80 and LC95 in ppm
3.5 Discussion
There is no baseline data on the susceptibility of P. xylostella to insecticides currently
available in South Africa. There are also no susceptible rearing colonies maintained which
can serve as reference colonies for toxicological studies. The results from this study,
therefore serve as baseline data for P. xylostella susceptibility to spinosad (spinosyn)
lambda–cyhalothrin (pyrethroid) and flubendiamide (diamide) in South Africa. Both P.
xylostella populations (B2018–01 and N2018–1) were highly susceptible to spinosad and
flubendiamide.
For flubendiamide P. xylostella exhibited high mortality levels > 80% at a low dosage (2.7
ppm) (Table 3.2), while the recommended dosage is 48 ppm. Resistance levels of P.
xylostella established by Liu et al. (2015) contradict the present study findings with 48.17–
fold resistance for chlorantraniliprole (diamide) with chlorantraniliprole also included in the
diamide group of insecticides.
Results from a study by Neto et al. (2016) indicated P. xylostella resistance to
chlorantraniliprole, spinosad and chlorfenapyr in Bezerros, Recife and Alegre. The LC50 (mg
a.i. /L) for spinosad in Recife was 0.017 compared to 3.64 in Bezerros with a resistance ratio
of 50 up to 200–fold (Neto et al., 2016). The LC50 and LC90 values for chlorpyrifos,
deltamethrin and spinosad were reported for P. xylostella populations from Kara and
Dapaong in Togo and Cotonou in Benin (Agboyi et al., 2016). These populations were
compared to a population from Kenya in Matuu as a control. Resistance to chlorpyrifos was
5 to 15–fold at LC50 and 9 to 885–fold at LC90 compared to the control population.
Deltamethrin had a 13 to 59–fold at LC50 and 149 to 1772–fold resistance at LC90 compared
to the control population (Agboyi et al., 2016). These P. xylostella populations were,
however, highly susceptible to spinosad (Agoyi et al., 2016). The estimates of the current
study for both populations tested, is in accordance with the findings of this study.
Kang et al. (2017) collected a P. xylostella population in Korea that exhibited 16.3–fold
resistance to chlorantraniliprole. After laboratory exposure to chlorantraniliprole for one year,
the resistance level increased to 2,157‐fold. This showed the ability of this pest to develop
resistance to insecticides (Kang et al., 2017). In an evaluation of various insecticide groups,
Kang et al. (2017) determined cross–resistance with only one diamide (flubendiamide)
showing 5,910 fold resistance (Kang et al., 2017). This resistant population did, however,
not show any cross–resistance to indoxacarb, spinetoram, metaflumizone and spinosad
(Kang et al., 2017). In this study, no–cross resistance was established between lambda–
cyhalothrin and any one of the other two insecticides evaluated, viz. spinosad, and
flubendiamide.
Sereda et al. (1997) reported a significant increase in P. xylostella populations on cabbage
in South Africa since 1995. In 1996, most populations sampled showed significant resistance
levels to deltamethrin (pyrethroid), methamidophos (organophosphate) and methomyl
(carbamate). Control failure for five out of six populations to deltamethrin was indicated at
the recommended dosage (RD) and double the RD rate by Sereda et al. (1997). Both the
populations tested in this study, N2018–01 and B2018–01, are also at risk of control failure
by lambda–cyhalothrin with the LC50, LC80 and LC95 for both populations found to be higher
than the recommended dosage. Sereda et al. (1997) stated that fewer larvae died after a
deltamethrin application compared to methamidophos and methomyl applied at RD and
double the RD. Resistance to deltamethrin at the RD was established in two populations,
Ventersdorp and Bloemfontein with 0% mortality (Sereda et al., 1997). Resistance by P.
xylostella to a pyrethroid (deltamethrin) was reported in South Africa in 1996. Sereda et al.
(1997) also reported less than 100% mortality of P. xylostella at the recommended dosages
for other deltamethrin, methamidophos and methomyl.
The long–term application of pyrethroids affects the effectiveness of this group, even after
application ceased. This, in turn, makes the introduction of new pyrethroids in a spraying
program, even based on rotation, obsolete (Sun et al., 1986). Plutella xylostella remains a
persistent and major pest of Brassicaceae with resistance development to insecticides a
reality. Control of this pest is also costly (Neto et al., 2016, Nauen and Staeinbach, 2016,
Kang et al., 2017). Populations from Nelspruit and Bapsfontein are still susceptible to
flubendiamide and spinosad. It is important to follow proper control programs where
insecticides with different modes of action are rotated to ensure effective control of P.
xylostella populations in South Africa.
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Chapter 4: Conclusion and recommendations
Brassicaceae (Cruciferae) comprises of a large number of frequently consumed vegetables.
The agricultural and economic importance of these vegetables is ascribed to their high levels
of minerals, polyphenols, antioxidants, vitamins and glucosinolates (Aires, 2015). Insects
are the most important crop pest with more than 10 000 species damaging crops worldwide.
However, only 700 inflict serious damage to crops in storage and in the field (FAO, 2019).
One of these is P. xylostella causing crop losses of up to 90% on cabbage (Verkerk and
Wright, 1996). Plutella xylostella is regarded as the most destructive pest of Brassicas
worldwide (Verkerk and Wright, 1996), with an estimated economic impact of US$4–5 billion,
if yield losses and control cost for all Brassicas are taken into account (Zalucki et al., 2012;
Bradshaw et al., 2016). Resistance development to insecticides by P. xylostella (Talekar
and Shelton, 1993; Nyambo and Löhr, 2005; Ayalew, 2006, Odhiambo et al., 2010, Santos
et al., 2011, Zhou et al., 2011; Agboyi et al., 2013 and Legwaila et al., 2014) in combination
with food safety have motivated the development of alternative management strategies
(Hooks and Johnson, 2003; Shelton and Badenes–Perez, 2006). The main focus of cultural
control is trap crops (Hooks and Johnson, 2003, Shelton and Badenes–Perez, 2006). The
most proposed trap crops for P. xylostella is yellow rocket (Barbarea vulgaris)
(Brassicaceae) and Indian mustard (Brassica juncea juncea) (Brassicaceae) (Charleston
and Kfir, 2000; Badenes–Perez et al., 2004; Lu et al., 2004; Shelton and Nault, 2004;
Badenes–Perez et al., 2005).
Choice and development tests conducted in this study indicated the use of Brassica juncea
var. integrifolia (Giant red mustard) very closely related to the already available trap crop,
Indian mustard (Brassica juncea juncea) as a viable trap crop for control of P. xylostella.
Mustard can be used as a trap crop for P. xylostella in cropping systems where tatsoi, pak–
choi, kale and cabbage are cultivated, since it was preferred to these crops for oviposition
and feeding by the pest in this study. Better control of P. xylostella can be achieved if
mustard as a trap crop can be integrated as part of an IPM system at Pico–Gro where these
crops are planted in greenhouses. Planting of mustard between other brassica crops such
as tatsoi, pak–choi, kale and cabbage, can reduce the number of individuals on the latter
crops if the trap crop is removed after infestation occurred. The continued planting of trap
crops like mustard and removing of infested trap crop plants as part of an IPM system may
reduce the population below the economic injury level.
Modern agricultural technology has allowed farmers to keep up with the need for food
security of a growing world population. Increased yields of major crops are achieved with
good cultivation practices and by applying pesticides (WHO, 2019). Although research on
P. xylostella has been done since the early 1900’s (Gunn, 1917), no comprehensive
integrated control strategy could be implemented for successful control of this pest. Despite
the efforts to establish integrated pest management, control strategies rely mainly on
insecticide application (Grzywacz et al., 2010). The pest status of P. xylostella can, however,
mainly be attributed to insecticide resistance and the absence of natural enemies in the
areas where host crops are cultivated (Taleker and Shelton, 1993). Arthropods cause 18–
20% of crop losses worldwide valued at US$470 billion (Sharma et al., 2017). To ensure
food safety on a global scale more than 1000 pesticides are currently used worldwide
against crop pests (FAO, 2019). It is possible to produce foods without the use of pesticides
in certain instances, however, these instances are rarely found. Compared to global
standards, maximum application rates of pesticides and frequencies of application are not
adhered to by southern African farmers (Williamson et al., 2008).
Plutella xylostella was the first crop pest to become resistant to DDT in the mid–1900’s
(Ankersmit, 1953) and also the first insect pest with resistance to Bacillus thuringiensis
(Tabashnik et al., 1990). Since 1995, Sereda et al., (1997), reported a significant increase
in P. xylostella populations on cabbage in South Africa. By 2011, P. xylostella showed
resistance to most insecticides applied under field conditions in certain cropping areas
(Ridland and Endersby, 2011) and also to new insecticide groups, including diamides,
spinosyns and phenylpyrazoles (Gong et al., 2014). This is, however, not the case in the
Nelspruit and Bapsfontein cropping areas with P. xylostella still being highly susceptible to
flubendiamide (diamide) and spinosad (spinosyns). In contrast, high levels of resistance in
P. xylostella populations sampled from these areas was found to lambda–cyhalothrin.
The possibility of resistance development to insecticides prompts more research of other
control methods (cultural, biological) for P. xylostella. The only viable solution is an IPM
program to ensure susceptibility to insecticides by P. xylostella as long as possible.
Therefore, continued research, especially in developing countries such as South Africa
remains important.
4.1 Recommendations
In this study, the potential to use mustard as a trap crop in integrated pest management of
P. xylostella was confirmed. It can thus be recommended to farmers to be integrated into
their IPM Systems for control of this pest. This aspect of the study can be expanded to
include more potential trap crops. It can then be applied in an area–wide IPM system for
control in heavily infested areas. Evaluation of the susceptibility of P. xylostella populations
to all registered insecticide groups must be continuously done according to the
recommended application set out on the label of the selected insecticides. This information
of frequently used insecticides can then be used to identify shifts in susceptibility.
The integration of trap crops and application of insecticides with the high efficacy of control
of P. xylostella can contribute to reducing the number of insecticide applications per season.
It can also prolong the effective use of these insecticides for control of P. xylostella in South
Africa.
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