MINISTRY OF EDUCATION
AND TRAINING

MINISTRY OF AGRICULTURE
AND RURAL DEVELOPMENT

VIETNAM ACADEMY OF AGRICULTURAL SCIENCES

DOAN THI LUONG

THE BIOLOGICAL AND ECOLOGICAL
CHARACTERISTICS AND CONTROL MEASURES OF
PSEUDO-MEALYBUG
Paracoccus marginatus Williams and Granara de Willink
(Homoptera: Pseudococidae)

CAUSING DAMAGE ON PAPAYA IN HANOI

Specialization : Plant protection
Code

: 9. 62. 01. 12

HA NOI - 2019


LIST OF THESIS-RELATED PUBLICATIONS
SUMMARY OF AGRICULTURE PhD THESIS
This thesis was completed at Vietnam
Academy of Agricultural Sciences


(Homoptera: Pseudococcidae) on papaya in bub-urban of
Hanoi ”, Journal of Agriculture and Rural development
(354+355)/ 2019, pages 310-319.


intercropped with maize was lower than that on monoculture papaya
(19.1 individuals/leaf and 1.32 individuals/fruit compared with 51.3
individuals/leaf and 5.4 individuals/fruit). P. marginatus on
monoculture papaya appeared earlier with density (256.5
individuals/leaf and 4.7 individuals/fruit) always higher than in
papaya rotated with sweet potato (72.1 individuals/leaf and 2.2
individuals/fruit).
1.5. Such cultivation techniques as rotation planting, intercropping
and high pressure watering on the leaves all have the effect of
limiting density of P. marginatus. The use of lower toxic chemicals
liked Spirotetramat and Pymetrozine (registered for mealybug on
fruit trees) is highly effective in the field (86.42% and 83.8%,
respectively). Rotenone, Abamectin and Petroleum spray oil
(registered to control mealybugs on fruit trees) which can provide
72% control of P. marginatus in the field condition, can be used
alternately with Spirotetramate and Pymetrozine for substitution of
chemical pesticides of toxic group 2 that farmers are using commonly
on papaya nowadays but not legally allowed to be used on fruit trees.
Spraying pesticides at 1st and 2nd instar nymphs of P. marginatus with
a minimum amount of water of 1000 liters/ha and spraying with
pressure compressing pump will bring optimal control.
II. Recommendations
Control of P. marginatus is real difficulty, so it is advised to
apply integrated measures as recommended in conclusion 1.4 and
the proper technique of pesticide use in conclusion 1.5 of this thesis

3. Scientific and practical significance
3.1. Scientific significance
The thesis provided scientific data on species composition of
mealybugs on papaya in Hanoi; providing basic biological and
ecological characteristics of P. marginatus and the effective control
measures to that insect in papaya growing areas of Hanoi.
3.2. Practical significance
The research findings of the thesis are the scientific basis to
develop an effective and environment sound protocol for control of
P. marginatus.
4. New research findings
- It is the first time recorded Paracoccus marginatus Williams
and Granara de Willink (Homoptera: Pseudococcidae) damaging

24

1


papaya in Vietnam
- Providing new scientific data on biological and ecological
characteristics, especially data on life table, population dynamic of
Paracoccus marginatus in Hanoi, hence updating systematically
scientific data on Paracoccus marginatus on papaya in Hanoi.
- Providing scientific data on the effectiveness of feasible
measures including cultivation, mechanical and chemical measures
for effectively and environmentally control of Paracoccus
marginatus on papaya in Hanoi.
5. The thesis structure
The thesis is structured in 151 pages, including introduction,

individuals/fruit) is significantly higher than that on dwarf variety
(28.2 individuals/leaf and 0.48-0.52 individuals/fruit). The density on
1–year-old papaya (255.0 -256.5 individuals/leaf and 6.5-7.3
individuals/fruit) is higher than that on 2–year-old papaya (53.1-53.8
individuals/leaves and 14,2-14,5 individuals/fruit). The density on
intercropped papaya is higher than that on monocultured papaya
(83.5 individuals/leaf and 13.2 individuals/fruit compared to 53.1
individuals/leaf and 4.26 individuals/fruit). The density on papaya
23


pesticides including Spirotetramate, Abamectin, Petroleum spray oil
and Pymetrozine with various sprayers such as hand compressing
sparyer, hand pre-compressed sprayer and motor compressed sprayer.
The result showed that when spraying with the conventional hand
compressing sprayer the efficacy of insecticides decreased
significantly compared to that when sprayed by pre-compressed
sprayer (49.70 - 62.87% compared to 68.88 - 81.98%). When
spraying by motor sprayer, the pesticide efficacy was not improved
even decreased compared to spraying with hand compressing sprayer
and pre-compressed sprayer.

22

Chapter 1
LITERATURE REVIEW AND SCIENTIFIC BACKGROUND
OF THESIS
1.1. Scientific background
The diversity of ecological and farming system (intensive,
intercropping, rotation, varieties and farming techniques) has a

1.2.2. Study on morphological characteristics of Paracoccus
marginatus
Morphological characteristics of adult, egg and nymph of P.
marginatus were described in Al-Helal et al. (2012), Mani
Chellappan et al. (2013b), Miller et al. (1999), Sharma et al. (2013),
Tanwar et al. (2010), Walker et al. (2003), Wu et al. (2014),...
1.2.3. Study on biological and ecological characteristics of
Paracoccus marginatus
Details of the biology and ecology of P. marginatus can be
found in the literature of Amarasekare et al. (2008a, 2008b),
Hintenou et al. (2015), Mani Chellappan et al. (2013b), Thangamalar
et al. (2010) and Walker et al. (2006).
1.2.4. Research on control of Paracoccus marginatus
Control of P. marginatus by integrated pest management
measures including phytosanitary, cultivation and manual, biocontrol with using botanical and chemical pesticides (Banu et al.,
2010; Galanihe et al., 2010; Krishnan et al., 2016; Mani et al., 2012;
Muniappan, 2014; Saengyot amd Burikam, 2011; Seni and
Chongtham, 2013; Sharma et al., 2013; Tanwar et al., 2010;…).
1.3. Research on Paracoccus marginatus on papaya in Vietnam
1.3.1. Detection of Paracoccus marginatus in Vietnam
P. marginatus was firstly recorded in Vietnam on cassava (Le
Thi Tuyet Nhung et al., 2014, 2015). So far there has been no
publication regarding this species on papaya.
1.3.2. Morphological characteristics of Paracoccus marginatus
Research results on the species composition of mealybugs
(Pseudococcidae) were published by Nguyen Thi Chat (2008),
Nguyen Thi Chat et al. (2005), Pham Van Lam (2013), Le Thi Tuyet
Nhung et al. (2018),… but very limitation of their morphological
characteristics were described.
1.3.3. Biological and ecological characteristics of Paracoccus

3.4.2.4. Efficacy of pesticides applied with different water volume to
control Paracoccus marginatus
The efficacy pesticides to control P. marginatus after 7 days of
spraying was highest when spraying at 1000 liters/ha compared to
600 and 800 liters/ha.
3.4.2.5. Efficacy of pesticides applied with different sparyers to
control Paracoccus marginatus
Experiments were conducted to investigate efficacy of 4

4

21


marginatus is significantly decreased compared to density in plot
washing at by compressor spraye rat 1000lit/ha in 1 day only.
Therefore, this method can be applied to manage P. marginatus when
the density is low.
3.4.2. Chemical application
The use of pesticides is a last measure when efforts to apply
other measures are not likely to prevent the outbreak of P.
marginatus. According to the list of pesticides allowed to be used in
Vietnam, issued together with the Ministry of Agriculture and Rural
Development’s Circular No. 03/2018 / TT-BNNPTNT dated
February 9, 2018, there are currently no pesticides registered to use
for control of P. marginatus on papaya. Meanwhile, in production,
farmers have to choose different types of mealybug on other crops,
including chemical pesticides belong to toxic group 2 that are not
allowed using to control mealybugs in fruit trees. This research has
focused on assessment of 14 pesticides, including 8 chemical

- Papaya growing areas in 03 communies of Hanoi: Phung
Thuong commune (Phuc Tho district), Dan Phuong commune (Dan
Phuong district), Di Nau commune (Thach That district).
- Research period: 2015 - 2018
2.2. Research content
- Surveying papaya insect pests and determining the main pests of
papaya in Hanoi.
- Determining biological and ecological characteristics of papaya
mealybug P. marginatus in laboratory.
- Study on population dynamic and factors affecting the population
density of P. marginatus on papaya in the study area.
- Research on IPM measures of P. marginatus on papaya.
2.3. Materials and tools for research
Materials
The source of P. marginatus used in the study was collected from
papaya orchards in Hanoi.
The Hong Phi - Taiwanese papaya variety was used to feed P.
marginatus in lab. experiments.
Two varieties (Hong Phi papaya – Taiwan and high yielding dwarf
papaya –Thailand) were used in field study.
Tools and equipments
Stereo microscope: Carl Zeizz Stemi 2000-C and microscope: Carl
Zeizz Promostar with a maximum magnification of 1000 times.
Air - controlled insect rearing chamber: DAEYANGETS model GC-101B
(RGX-400E brand) with temperature, humidity and light control system. Other


laboratory equipment: insect-proof plastic boxs, petri boxes, tubes, insect needles,
lame, lamen, plastic pots, insect netting cages, green houses, quills, blotting paper,
sample containing jars, nylon bags,...


3.3.4. Effect of rotation on the density of P. marginatus on papaya
In Thach That, farmers usually grow monoculture papaya or 1
year old papaya rotated with potatoes, chilli, vegetables, etc.
Observation showed that in monoculture gardens, P. marginatus
began to appear on leaves from 5 March 2017 with a low density, an
average of 0.8 individuals/leaf. Then increased, especially increasing
rapidly from mid-April and peaking first time from 29 June 2017 to 6
July 2017 (with 39.3 - 39.8 individuals/leaf, 4.8 - 6.3
individuals/fruit) and second time at 19 October 2017 (with 256.5
individuals/leaf, 4.7 individuals/fruit). When rotation with potato, P.
marginatus started to appear on papaya leaves later with lower
density (0.30 individuals/leaf) and then increased rapidly from the
end of April and the get the first peak from 29 June 2017 to 6 July
2017 (with 21.3 - 22.5 individuals/leaf, 2.9 - 3.5 individuals/fruit)
and second pick at 19 October 2017 (with 72.1 individuals/leaf, 2.2
individuals/fruit).
3.4. IPM measures of Paracoccus marginatus damage on papaya
3.4.1. Cultivation measures
3.4.1.1. Using tolerant varieties
The surveillence indicated that density of P. marginatus on the
high yielding dwarf variety is significantly lower than that on Hong Phi
variety. So that, using dwarf papaya variety is advised to limit the
density and damage of P. marginatus, hence limitation use of pesticides.
3.4.1.2. Intercropping
It was also found from population dynamic study that when
intercropping with maize, the density of P. marginatus was much
lower than that of monoculture gardens, while the density of P.
marginatus in intercropping with bananas was higher than that of
monoculture papaya. Thus, to limit the damage of P. marginatus,

29 June 2017 at 16.2 individuals/leaf, 1.6 individuals/fruit, and on 2
Nov. 2017 at 53.1 individuals/leaf, 4.26 individuals/fruit).
When applying maize intercropped in papaya garden at Thach
That, P. marginatus population during the period from January to
mid-May was low, averaging of 2.2 - 5.5 individuals/leaf, 0.1 - 1.3
individuals/fruit. After that, the density began to increase, forming
two peaks: pick 1 from June 22 to June 29 2017 (with 8.7 - 9.5
individuals/leaf, 0.8 - 1.96 individuals/fruit), and pick 2 at November
9 2017 (with 19.1 individuals/leaf, 1.32 individuals/fruit),
significantly lower than the density in monoculture orchard (peak 1
from June 22 to 29 2017 at 16.1 - 16.2 individuals/leaf, 8.7 - 9.5
individuals/fruit, and peak 2 on November 2 2017 at 51.3
individuals/leaf, 5.4 individuals/fruit).

the life cycle; population development criteria such as net
reproductive rate (Ro), the intrinsic rate of increase (Rm), the finite rate
of increase (λ), mean generation time (Tc) and doubling time (DT),
and adjusted with formular of Birch (1948) and Kakde et al. (2014).
2.4.3. Method of studying on population dynamic and factors
affecting the population densities of Paracoccus marginatus
Carried out on two papaya varieties: Hong Phi (Taiwan) and
high yielding dwarf (Thailan) at various conditions suchs as: plant
age (1 year and 2 years old); planting mode (monoculture,
intercroping and rotating with potato). Observation was followed
survey method of Plant Protection Research Institute (1997).
2.4.4. Method for research on IPM measures of Paracoccus
marginatus on papaya
2.4.4.1. Research on cultivation measures
The research was conducted with 3 control measures including
(i) using resistant papaya varieties (Hong Phi and high yielding dwarf

Adjusting the efficacy by the Abbot formula for Lab. tests and
Henderson-Tilton formula for field trials.
2.5. Data statistix methods
Field data were statistixed with Excel and statistical Window
software.
CHAPTER 3
FINDINGS AND DISCUSSION
3.1. Species composition of papaya pests and main pests damaged
papaya in Ha Noi
3.1.1. Species composition of insect and mite pests damaging papaya
Have been 8 species belonging to 8 different families of 6 insect
and mite orders collected and identified, similar to the number of insects/
mites found on the papaya in Vietnam until 2013 (Pham Van Lam,
2013). However, the majority of insect species (6 species) in this study
did not coincide with those recorded on papaya before 2013.
3.1.2. Identifying the scientific names of pests collected on papaya
It was showed by using the taxonomy keys of Williams (2004),
Williams and Watson (1988) that the characteristics of the mealybug
species collected on papaya in Hanoi belonging to genus of Paracoccus
Ezzat & Mc Connell. Folloing the identification key of Williams and
Willink (1992), the mophology characteristics observed on Lam
sampled, are coincided with characteristics of P. marginatus Williams
and Granara de Willink species (Figure 3.1). After identification,
specimen of mealybug species was sent to the Pest Identification Center
of the California Department of Agriculture and Food for re8

3.3. The population dynamic and factors affecting the density of
Paracoccus marginatus on papaya in the study area
3.3.1. Population dynamic of Paracoccus marginatus on papaya
The survey showed that on high yielding dwarf papaya variety,

17


26 days age, then starting to reduce with laying time. The last fecundity
day of female adult is 41 days age (Figure 3.12).

Hình 3.12. Age specific survival rate (lx), age specific fecundity
(mx) of P. marginatus at 30oC and 80% RH
Rearing at a temperature of 25°C, 80%RH, a photoperiod of
16L:8D with papaya leaves as food, the population growth parameters
of P. marginatus including Ro, Rm, λ, Tc and DT reached 457.87 ♀/♀,
0.188 ♀/♀/day, 1.19 times, 34.71 days and 3.93 days, respectively.
When rearing at 30°C with the same humidity and food, depending on
each parameter, its value reached at 367.79 ♀/♀, 0.197 ♀/♀/day, 1. 22
times, 28.17 days and 3.52 days, respectively (Table 3.16).
Table 3.16. Population growth parameters of P. marginatus at
various constant temperatures (in Plant Protection Research Institute)
Testing
Giá trị các thông số bảng sống
conditions
Ro
rm
λ
Tc
DT
25ºC, 80%RH
457,87 0,188 1,19 34,71 3,93
30ºC, 80%RH
367,79 0,197 1,22 28,17 3,52
3.2.2.8. The number of generations per year of Paracoccus marginatus

Nymph: newly hatched nymph (first instar nymph) is an ovalshaped body, yellowish green, indistinguishable by sex. The size is quite
small, the body is only 0.5 ± 0.01 mm long and the widest part of the
body is only 0.21 ± 0.01 mm (Figure 3.3).

9


Figure 3.3. The 1st instar nymph of P. marginatus
2 instar nymph of P. marginatus is quite a clear distinction in
color and shape of female sex and male sex. 2nd instar nymph of female
sex is indistinguishable by shape and color from that of 1st instar nymph
(Figure 3.4b). The body of a 2nd instar nymph of female sex has a length
of 0.84 ± 0.021 mm and the width is 0.43 ± 0.01 mm. The 2nd instar
nymph of male sex gradually changes from yellowish-green to a pale
pink, then gradually darkens to a deep red with the body length of 1.2 ±
0.05 mm and the width of 0.61 ± 0.02 mm (Figure 3. 4a).
nd

male sex is 89.41-93.02% and at nymph stage in female sex is 89.4196.77%. The survival rate at pre-pupa and pupa stages, respectively,
are 87.5-95.83% and 85.71-93.48%. The survival rate of whole stage
(from egg to male) rearing at a temperature of 25°C was significantly
higher than that at 30°C, and reached 76.79% and 62.5%,
respectively. The survival rate at whole stage from egg to female is
equivalent at two experimental temperatures, reached 81.83% at
25°C and 81.08% at 30°C. This result is similar to studies of
Amarasekare et al. (2008a, 2008b).
3.2.2.7. Live table of Paracoccus marginatus
Rearing at 25ºC, 80%RH, photoperiod of 16L:8D and feeding
with papaya leaf, the age specific survival rates (lx) of P. marginatus
adult is 100% at 34 days age. From 35 days age, lx is starting to

when rearing at 25oC and 30oC, at P
marginatus
marginatus
3.2.2. Biological and ecological characteristics of Paracoccus
marginatus
3.2.2.1. Habitat of Paracoccus marginatus
P. marginatus lives on all upper parts of the papaya (leaves,
buds, flowers, fruits, young parts of the stem). On opened papaya
leaves, P. marginatus mainly lives on the underside, near the petiole,
the main veins of the leaves. Females without wings, move by
crawling for short distances or are carried with the wind. 1st instar
nymph is easily spread by wind, workers’ cloth and tools. 1st instar
nymph plays a very important role in the spread of P. marginatus in
the field. Other instar nymphs are immobile. The body of nymphs
and adults of P. marginatus is always covered with a layer of white
wax powder like cotton. The observation of the living behavior of P.
marginatus in this thesis are similar to the research findings of many
authors (Seni and Chongtham, 2013; Tanwar et al., 2010; etc.).
3.2.2.2. Metamorphic characteristics of Paracoccus marginatus
When rearing at stable conditions (25°C, 30°C; 80% RH; and a
photoperiod of 16L:8D) and Taiwan's papaya leaves food, P. marginatus
has two types of metamorphosis depending on sex. The female has the
style of hemimetamorphosis whereas the male has the style of
hypermorphosis (the hypermorphosis has some phases, including egg,
nymph, pre-pupa, pupa and adult). Nymph developed to female adult
has 3 instars while nymph developed to male adult has 2 instars only.
This metamorphosis of P. marginatus was showed as other pseudomealybug species and it is specific metamorphosis of
Pseudococcidae (Борxceниуc, 1963; Kosztarab and Kozar, 1988).
12

3.2.2.3. Life cycle of Paracoccus marginatus

6,13±0,06 b (6-7)
8,63±0,33 b (6-15)
1,20±0,09 b (1-3)
1,83±0,08 b (1-3)
17,80±0,35 b (14-24)

Table 3.8. Development times in female sex of P. marginatus under
laboratory conditions (in Plant Protection Research Insitute)
Development time (days) in conditions
Phases/stages
25oC, 80% RH
30oC, 80% RH
Egg
7,33±0,08 a (7-8)
6,10±0,06 b (6-7)
Nymph
Pre-oviposition period
Egg-female
Life cycle

16,22±0,32 a (13-22)
7,06±0,33 a (5-10)
23,56±0,33 a (20-29)
30,31±0,52 a (25-36)

13

13,93±0,30 b (11-17)
5,69±0,20 b (4-7)
20,03±0,31 c (17-23)