You are on page 1of 647

M.Mani C.

Shivaraju Editors

and their
Management in
Agricultural and
Horticultural crops
Mealybugs and their Management
in Agricultural and Horticultural crops
M. Mani C. Shivaraju

Mealybugs and their

Management in
Agricultural and
Horticultural crops
M. Mani C. Shivaraju
Indian Institute of Horticultural Research Indian Institute of Horticultural Research
Bangalore, India Bangalore, India

ISBN 978-81-322-2675-8 ISBN 978-81-322-2677-2 (eBook)

DOI 10.1007/978-81-322-2677-2

Library of Congress Control Number: 2016930104

Springer New Delhi Heidelberg New York Dordrecht London

Springer India 2016
This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or
part of the material is concerned, specically the rights of translation, reprinting, reuse of
illustrations, recitation, broadcasting, reproduction on microlms or in any other physical way,
and transmission or information storage and retrieval, electronic adaptation, computer software,
or by similar or dissimilar methodology now known or hereafter developed.
The use of general descriptive names, registered names, trademarks, service marks, etc. in this
publication does not imply, even in the absence of a specic statement, that such names are
exempt from the relevant protective laws and regulations and therefore free for general use.
The publisher, the authors and the editors are safe to assume that the advice and information in
this book are believed to be true and accurate at the date of publication. Neither the publisher nor
the authors or the editors give a warranty, express or implied, with respect to the material
contained herein or for any errors or omissions that may have been made.

Printed on acid-free paper

Springer (India) Pvt. Ltd. Springer is part of Springer Science+Business Media (www.springer.
Dedicated to my wife Vijayarani who was
involved with the work on mealybugs.
She had helped me to carryout extensive
surveys for mealybugs in different crops in
India. She has also played a major role in
nalising the draft on Mealybugs and their
Management in Agricultural and
Horticultural crops.

Crop protection in the present day is as important as crop production. Pests

have plagued mankind from the beginning and will continue to vex the people
and thwart all their endeavors to the end. Mealybugs are sap-sucking insects
named for the powdery secretions covering the bodies. Mealybugs are soft-
bodied insects covered with waxy coating. They are sessile insects. They are
phloem feeders and suck the sap from all plant parts and also transmit some
plant disease thus causing serious economic losses to economically important
crop plants. Many of the mealybugs are arboreal and some are subterranean
feeding on the roots. They are windblown, and the spreading of mealybugs is
facilitated by wind. Within 2 days of hatching, they are also covered by waxy
coating making them hard to get killed with chemicals. Hence they are called
as hard to kill insects.
Mealybugs mostly live in protected habitats. They are found in cracks,
crevices inside the fruit clusters, lower surface of the leaves, etc. Since they
live in concealed plant parts, the chemicals will not reach the target pests
making chemical control ineffective. Many a time, mealybugs become abun-
dant in the fruiting phase of the plants. Several applications of insecticides are
needed for mealybug control. Thus frequent application of insecticides for
mealybug control leads to residue problem on the fruits, making unt for
export and hazardous to domestic market.
This book covers all the basic and applied aspects of the mealybug species
ultimately useful to implement the integrated mealybug management in differ-
ent agricultural crops. The book covers the information on identication of the
mealybugs, morphology, cytogenetics, taxonomy, molecular characterization
for identication, biology, damage, mealybugs as vectors, seasonal develop-
ment, natural enemies, culturing of mealybugs, ant association, control mea-
sures, insecticide resistance and mealybug management in different crops.
This book on Mealybugs and their Management in Agricultural and
Horticultural crops is rst of its kind since there is no comprehensive book
covering all aspects of mealybug available in the world. This will serve as a
guide for crop growers, state goverment ofcials and other stake holders
industry, besides researchers and students engaged in mealybug research and
development activities.

Indian Council of Agricultural Research N.K. Krishna Kumar

New Delhi 12, India,
July, 2014


Mealybugs throughout the world cause a variety of economic problems. The

most obvious damage is caused by the sucking habits of these insects. Heavy
infestations often cause stunting or death to the plant host. At times, mealy-
bugs have toxins and act as vectors of certain viruses detrimental to plant life.
Information on morphology, cytogenetics, taxonomy, molecular charac-
terization for identication, morphology, biology, damage, mealybugs as vec-
tors, seasonal development, natural enemies, culturing of mealybugs, ant
association, control measures, insecticide resistance etc are covered in this
book. It also deals with the all the mealybug management practices, which
include monitoring of mealybugs, use of pheromones, cultural practices,
chemical control and biological suppression available in the world.
We tried to accommodate almost all the important information generated
on the mealybugs up to 2014. A complete list of mealybug occurring in dif-
ferent crop growing regions of the world is also covered in this book, which
will be ready reckoner for the crops. We sincerely hope that this book will
provide useful information to many entomologists and students working on
mealybugs. It is a pleasure to thank all those people who gave help, sugges-
tions and encouragement in the preparation of our book Mealybugs and their
Management in Agricultural and Horticultural crops.

Bangalore, Karnataka, India M. Mani

C. Shivaraju


The beatitude and euphoria that accompanies successful completion of any

task would be incomplete without the expression of appreciation of simple
certitude to the people who made it possible to achieve the goal by their
encouragement and support. We heartily thank Dr. N. K. Krishnakumar,
Deputy Director General of Horticulture, Indian Council of Agricultural
Research, New Delhi, for his technical guidance. We are immensely grateful
to Dr. Amrik Singh Sidhu, Director, Indian Institute of Horticultural Research,
Bangalore, for his genuine guidance, impeccable and scholarly advice, recur-
ring encouragement, sustained interest and above all his affectionate way of
dealing with things throughout the course of writing the book. We wish to
express our extreme and profound sense of gratitude to Dr. Ameriksingh
Siddu, Director, Indian Institute of Horticultural Research, Bangalore.
Karnataka, India, for his valuable suggestions and useful guidance. We take
this opportunity to convey our sincere thanks to Dr. Abraham Verghese,
Director, National Bureau of Agriculturally Important Insects Resource,
Bangalore, for the encouragement to write this book.


1 Introduction ................................................................................... 1
M. Mani and C. Shivaraju

Part I Mealybugs

2 Morphology ................................................................................... 7
M. Mani and C. Shivaraju
3 Cytogenetics ................................................................................... 19
Ramakrishna Sompalaym, Kokilamani A. Lingarajaiah,
Raju G. Narayanappa, Jayaprakash,
and Venkatachalaiah Govindaiah
4 Taxonomy ....................................................................................... 55
M. Mani
5 Molecular Identification of Mealybugs ....................................... 75
K.B. Rebijith, R. Asokan, and N.K. Krishna Kumar
6 Biology............................................................................................ 87
M. Mani and C. Shivaraju
7 Culturing of Mealybugs ................................................................ 107
M. Mani and C. Shivaraju
8 Mode of Spread of Mealybugs ..................................................... 113
M. Mani and C. Shivaraju
9 Damage........................................................................................... 117
M. Mani and C. Shivaraju
10 Mealybugs as Vectors .................................................................... 123
R. Selvarajan, V. Balasubramanian, and B. Padmanaban
11 Economic Importance................................................................... 131
M. Mani and C. Shivaraju
12 Ecology ........................................................................................... 141
M. Mani and C. Shivaraju
13 Natural Enemies of Mealybugs .................................................... 149
A.N. Shylesha and M. Mani

xiv Contents

14 Semiochemicals in Mealybugs...................................................... 173

N. Bakthavatsalam
15 Ant Association .............................................................................. 199
M. Mani and C. Shivaraju
16 Methods of Control ....................................................................... 209
M. Mani and C. Shivaraju
17 Insecticide Resistance and Its Management in Mealybugs ....... 223
T. Venkatesan, S.K. Jalali, S.L. Ramya, and M. Prathibha
18 Mealybug Alikes ............................................................................ 231
M. Mani and Shaheen Gul

Part II Management of Mealybugs in Agricultural

and Horticultural Crops

19 Rice ................................................................................................. 239

Gururaj Katti
20 Wheat ............................................................................................. 247
Srinivasa Babu Kurra, Jeyakumar Ponnuraj,
and Shyam Prasad Gogineni
21 Barley ............................................................................................. 249
M. Mani
22 Groundnut ..................................................................................... 251
G. Harish and M.V. Nataraja
23 Sunflower ....................................................................................... 257
K.S. Jagadish, Chandrashekar, H. Basappa,
G. Basana Gowda, and Y.G. Shadakshari
24 Pulses .............................................................................................. 263
S.K. Singh, S.D. Mohapatra, and P. Duraimurugan
25 Soybean .......................................................................................... 267
M. Mani
26 Cotton ............................................................................................. 271
V.S. Nagrare, S. Kranthi, Rishi Kumar, B. Dharajothi,
M. Amutha, and K.R. Kranthi
27 Jute and Allied Fibre Crops ......................................................... 283
M. Mani and S. Satpathy
28 Sugarcane....................................................................................... 287
R. Jayanthi, J. Srikanth, and S.N. Sushil
29 Fruit Crops: Apple ........................................................................ 297
M. Mani
30 Fruit Crops: Pears ........................................................................ 303
M. Mani
Contents xv

31 Fruit Crops: Plum ......................................................................... 307

M. Mani
32 Fruit Crops: Peaches .................................................................... 311
M. Mani
33 Fruit Crops: Persimmon .............................................................. 313
M. Mani
34 Fruit Crops: Passion Fruit ........................................................... 317
M. Mani
35 Fruit Crops: Apricot ..................................................................... 319
M. Mani
36 Fruit Crops: Pistachio and Almond ............................................ 321
M. Mani
37 Fruit Crops: Strawberry .............................................................. 327
M. Mani
38 Fruit Crops: Grapevine ................................................................ 329
M. Mani and U. Amala
39 Fruit Crops: Citrus ....................................................................... 353
C.N. Rao, V.J. Shivankar, K.J. David, M. Mani,
and A. Krishnamoorthy
40 Fruit Crops: Guava ....................................................................... 377
M. Mani
41 Fruit Crops: Mango ...................................................................... 385
M. Mani
42 Fruit Crops: Papaya ..................................................................... 395
M. Mani, M. Kalyanasundaram and C. Shivaraju
43 Fruit Crops: Pineapple ................................................................. 411
M. Mani
44 Fruit Crops: Avocado .................................................................... 419
M. Mani
45 Fruit Crops: Banana ..................................................................... 423
B. Padmanaban and M.M. Mustaffa
46 Fruit Crops: Sapota ...................................................................... 429
M. Mani
47 Fruit Crops: Pomegranate ........................................................... 433
M. Mani
48 Fruit Crops: Ber ............................................................................ 439
M. Mani
xvi Contents

49 Fruit Crops: Custard Apple ......................................................... 443

M. Mani
50 Fruit Crops: Phalsa....................................................................... 447
M. Mani
51 Fruit Crops: Litchi ........................................................................ 449
M. Mani
52 Fruit Crops: Jackfruit .................................................................. 451
M. Mani
53 Vegetable Crops ............................................................................. 455
A. Krishnamoorthy and M. Mani
54 Tuber Crops ................................................................................... 471
M. Mani, M. Kalyanasundaram, C.A. Jayaprakas,
E.R. Harish, R.S. Sreerag, and M. Nedunchezhiyan
55 Ornamental Plants ........................................................................ 495
V. Sridhar, L.S. Vinesh, and M. Mani
56 Orchids ........................................................................................... 525
N.K. Meena, R.P. Medhi, and M. Mani
57 Medicinal Plants ............................................................................ 535
V. Sridhar, L.S. Vinesh, and M. Mani
58 Plantation Crops ........................................................................... 543
Chandrika Mohan, P. Rajan, and A. Josephrajkumar
59 Rubber ........................................................................................... 557
Mani Chellappan
60 Cashew ........................................................................................... 561
V. Ambethgar
61 Oil Palm ......................................................................................... 569
P. Kalidas
62 Spices .............................................................................................. 573
S. Devasahayam and T.K. Jacob
63 Mulberry ........................................................................................ 579
J.B. Narendra Kumar, M.A. Shekhar, and Vinod Kumar
64 Tobacco .......................................................................................... 589
M. Mani and G.N. Rao
65 Jatropha ......................................................................................... 591
M. Mani
Contents xvii

66 Forage Crops and Grasses ........................................................... 595

Narendra S. Kulkarni and M. Mani
67 Forest Plants .................................................................................. 607
R. Sundararaj and M. Mani
68 Glasshouse, Greenhouse and Polyhouse Crops .......................... 621
K. Gopalakrishna Pillai
69 Root Mealybugs ............................................................................. 629
Maicykutty Mathew and M. Mani
70 Coffee ............................................................................................. 643
P.K. Vinod Kumar, G.V. Manjunath Reddy, H.G. Seetharama,
and M.M. Balakrishnan
List of Tables

Table 4.1 List of mealybug species with eld-identifying

characters with their respective images .............................. 59
Table 4.2 List of mealybug species, correct identity of which
led to a successful biological control. ................................ 72
Table 5.1 Primers employed in DNA barcoding of mealybugs ......... 80
Table 5.2 Maximum composite likelihood estimate
of the pattern of nucleotide substitution from
29 species of mealybugs..................................................... 81
Table 10.1 Mealybug transmitted plant viruses ................................... 127
Table 13.1 List of predators recorded on the mealybugs ..................... 154
Table 13.2 List of some important encyrtid parasitoids
of mealybugs ...................................................................... 166
Table 13.3 List of entomopathogens and entomopathogenic
nematodes recorded on mealybugs .................................... 168
Table 14.1 Pheromone compounds identied from different
species of mealybugs.......................................................... 178
Table 19.1 List of mealybug species recorded on rice
in different regions of the world ......................................... 240
Table 20.1 List of mealybugs recorded on wheat ................................ 248
Table 22.1 List of mealybugs reported on groundnut
in different countries .......................................................... 252
Table 24.1 List of mealybugs recorded on pigeon pea......................... 264
Table 25.1 List of mealybugs recorded on soybean ............................. 268
Table 26.1 Mealybug species recorded on cotton in different
regions of the world............................................................ 272
Table 27.1 List of mealybugs recorded on Kapok
in different countries .......................................................... 284
Table 28.1 List of mealybugs recorded on sugarcane
in different regions of the world ......................................... 288

xx List of Tables

Table 29.1 List of mealybug species infecting apple

in different regions of the world ......................................... 298
Table 30.1 List of mealybugs recorded on pears
in different countries .......................................................... 304
Table 38.1 Mealybug species recorded on grapevine
in different regions of the world ......................................... 330
Table 38.2 List of insecticides recommended to control
mealybugs .......................................................................... 340
Table 39.1 List of mealybug species recorded on citrus
in different regions of the world ......................................... 354
Table 40.1 List of mealybugs recorded on guava
in different countries .......................................................... 378
Table 41.1 List of mealybugs recorded on mango
in different countries .......................................................... 386
Table 42.1 List of mealybugs recorded on papaya
in different regions of the world ......................................... 396
Table 42.2 List of natural enemies on Paracoccus
marginatus .......................................................................... 400
Table 43.1 List of mealybugs recorded in pine apple
in different countries .......................................................... 412
Table 45.1 List of mealybugs recorded on banana
in different countries .......................................................... 424
Table 46.1 List of mealybugs recorded on sapota
in different countries .......................................................... 430
Table 47.1 List of mealybugs recorded on pomegranate
in different regions of the world ......................................... 434
Table 48.1 List of mealybugs recorded on ber
in different countries .......................................................... 440
Table 49.1 List of mealybugs recorded on custard apple
in different countries .......................................................... 444
Table 51.1 List of mealybugs recorded on Litchi
in different countries .......................................................... 449
Table 52.1 List of mealybugs recorded on Jackfruit
in different regions ............................................................. 452
Table 52.2 Nipaecoccus viridis and its natural enemies
on Jack fruit ........................................................................ 452
Table 53.1 List of mealybugs recorded on tomato
in different countries .......................................................... 456
List of Tables xxi

Table 53.2 List of mealybugs recorded on eggplant ............................ 458

Table 53.3 List of mealybugs recorded on okra in
different countries .............................................................. 461
Table 53.4 List of mealybug occurring on different
vegetable crops ................................................................... 464
Table 54.1 List of mealybug species reported on cassava
in different regions ............................................................. 472
Table 54.2 List of natural enemies recorded on P. manihoti,
F.virgata, and Ph.solenopsis infesting cassava................... 476
Table 54.3 List of mealybugs recorded on tuber crops
other than cassava............................................................... 487
Table 55.1 List of some mealybugs recorded on different
ornamental plants ............................................................... 496
Table 56.1 List of mealybugs reported on orchids
in different regions ............................................................. 526
Table 57.1 Various medicinal and aromatic plants infested
with different mealybugs .................................................... 538
Table 58.1 Mealybugs recorded on Palms ........................................... 544
Table 58.2 List of mealybugs recorded on cocoa
in different countries .......................................................... 550
Table 58.3 List of mealybugs recorded on tea ..................................... 554
Table 59.1 List of mealybugs recorded on rubber
in different countries .......................................................... 558
Table 60.1 List of mealybugs recorded on cashew
in different countries .......................................................... 562
Table 61.1 List of mealybugs recorded on oil palm
in different countries .......................................................... 570
Table 62.1 List of mealybug species recorded on
different spice crops ........................................................... 574
Table 63.1 List of mealybug species recorded on mulberry
in different regions in the world ......................................... 580
Table 64.1 List of mealybugs recorded on tobacco.............................. 590
Table 66.1 List of mealybugs attacking the grasses
and fodder crops ................................................................. 596
Table 67.1 List of mealybug species infesting
different forest plants ......................................................... 614
Table 69.1 List of other root mealybugs on different
host plants in different countries ........................................ 630
Table 70.1 List of mealybugs recorded on coffee from
different countries .............................................................. 644
About the Editors

Dr. M. Mani is an agricultural scientist with over

35 years of R&D experience in the entomological
research. He has served in Indian Council of
Agricultural Research and Tamil Nadu Agricultural
University. His focal subject is pest control in hor-
ticultural crops including grapes. He has done work
on mealybugs for 35 years. Currently, he is an
Emeritus Professor of ICAR, New Delhi. He got
seven awards including lifetime achievement for
his contribution to the research in horticulture ento-
mology. He is associated with ve scientic bodies.
The author has published two books in 2013: (1) A Wonder Predator
(Cryptolaemus) by Lap Lambert Academic Publishing Company, Germany
(2) The Grape Entomology by Springer.

Dr. C. Shivaraju has worked extensively on insects

infesting several agricultural and horticultural
crops in Indian Institute of Horticultural Research
and National Bureau of Agriculturally Important
Insects both located at Bangalore. Particularly, he
contributed signicantly in research on eucalyptus
and papaya pest management. He has co-authored
two books: A Wonder Predator (Cryptolaemus) and
The Grape Entomology.

M. Mani and C. Shivaraju

Mealybugs belong to the insect group that is fungus called sooty due to which a signicant
commonly known as scale insects; They have infestation of mealybug creates a black, sticky
soft segmented oval bodies, but without an outer mess. Most of the economically important mealy-
shell. Mealybugs (Hemiptera, Sternorrhyncha, bug species are known to be associated with
Coccoidea, Pseudococcidae, and Putoidae) are long lists of host plants, and the development of
small, soft-bodied plant sap-sucking insects. The high population density, which eventually would
name mealybug is descriptive of the insects kill the host plant. Plant growth conditions may
body, which is covered by a white sticky powder strongly affect the development of the mealybug.
resembling cornmeal. Their common name is Flowering and fruiting phases of plant support
derived from the mealy wax secretion that usu- heavy mealybug population. Likewise, hot
ally covers their bodies (Kosztarab and Kozr weather favors rapid multiplication resulting in
1988). Because of their appearance, mealybugs the outbreak of mealybug population.
are often confused for cushionscale insects or Many of the mealybugs show sexual dimor-
woolyaphids. Unlike their close relative scale phism but parthenogenetic mode of reproduction
insects, mealybugs retain their legs throughout is also observed in some species of mealybugs.
their lives. Mealybugs may be oviparous or viviparous or
Mealybugs feed on a variety of herbaceous ovoviparous. The eggs are usually laid in loose
and woody plants, including the angiosperm, masses of cottony wax or felt-like ovisacs. Some
gymnosperm, and fern families. Most of the species bear living young. Only newly hatched
mealybugs are arboreal and some are subterra- mealybugs, also called as crawlers, are not cov-
nean feeding on the roots. They are phloem feed- ered with wax coating, moving from one part to
ers and suck the sap from all plant parts and also another within the plant and also between plants;
transmit some plant disease, thus causing serious this is the most vulnerable stage for chemical
economic losses to economically important crop control. They are windblown, and the spreading
plants. Mealybugs take in great quantities of plant of mealybugs is facilitated by wind. Within two
uids and therefore excrete a lot of liquid waste days, they are also covered by waxy coating,
called honey that supports the growth of a black making them hard to get killed with chemicals.
There are three nymphal instars in female and
four in male mealybugs also covered with wax.
M. Mani (*) C. Shivaraju
Adult male and female mealybugs are completely
Indian Institute of Horticultural Research,
Bangalore 560089, India different from each other. Adult female mealy-
e-mail: bugs are characteristically elongate, oval, soft,

Springer India 2016 1

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_1
2 M. Mani and C. Shivaraju

and with distinct segmentation measuring as some chemicals to be unsustainable. Furthermore,

much as 89 mm in length. They are wingless many of these products are increasingly unac-
and their mouthparts are thread-like, inserting ceptable because of their human toxicity and low
through the plant tissue to suck juices from the selectivity; some are no longer available and oth-
host, thereby causing damage. The adult male ers are targeted for reduction under national pro-
has a pair of long opaque wings, slender body, grams and regulations for sustainable use of
and two multisegmented antennae that are about pesticides, in light of their risk or hazard assess-
half the body length and a pair of halters with ments (Charles et al. 2006; Franco et al. 2004;
hooks. It bears two white, long anal laments. Walton et al. 2006). Since they live in concealed
Adult males are about 1.5 mm in length. They are plant parts, the chemicals will not reach the target
active iers but have abortive mouthparts and pests, often making chemical control ineffective.
take no food. Their role in life is to y and nd a Many a time, mealybugs become abundant in the
female to mate. Females release a pheromone to fruiting phase of the plant. Multiple applications
attract the winged males. Females are abundant of insecticides are needed for their control. Thus,
in elds while male mealybugs are so rarely frequent application of insecticides for mealybug
available. They reproduce sexually and partheno- control leads to residue problem on the fruits
genetically. The males, seldom seen, are delicate. making them unt for export and hazardous to
Outwardly, mealybug species look similar. domestic market.
However, each species has distinct biological However, mealybugs have a very rich natural
and morphological characters. Identication enemy complex. Biological control of mealybugs
of mealybugs is based upon adult females. is widely recommended. It includes several gen-
They constitute the second largest family of eral predators like coccinellids, chrysopids,
Coccoidea, with more than 2000 described lycaenids, drosophilids, and cecidomyiids.
species and ca. 290 genera (Ben-Dov 2006; Mealybugs are known to be attacked by several
Downie and Gullan 2005). parasitoids, mainly the encyrtids and some other
Economic losses resulting from mealybug parasitoids like aphlelinids, platgasterids, braco-
infestations have increased over a period of years. nids, pteromalids, eulopids, eucilids, and sig-
In response, there has been a cosmopolitan effort niphorids. Many are host specic and very
to improve control strategies and better under- effective against mealybugs. In the case of undis-
stand mealybug biology and ecology as well as turbed or uninterrupted broad-spectrum and del-
their role as vectors of plant pathogens (Daane eterious chemicals, the local natural enemies play
et al. 2012). an important role in the population regulation of
For the most part in their life stages, mealy- mealybugs. Many a time, the local natural ene-
bugs are covered with waxy coating, including mies appear a little late when mealybug popula-
eggs, making the control with chemicals difcult. tion reaches very high numbers. Some local
Mealybugs mostly live in protected habitats. natural enemies have their own limitations like
They are found in cracks, crevices inside the fruit hyperparasitism or reach a biotic balance.
clusters, lower surface of the leaves, etc. Hence Addition of these local natural enemies to the
they are called as hard to kill insects. crop ecosystem may not enhance the natural par-
Chemical control is still the most common asitism or predation to bring down the mealybug
control tactic used against mealybug pests. population effectively. Exotic natural parasitoids/
However, the cryptic behavior of mealybugs, predators from other countries help extensively
their typical waxy body cover, and clumped spa- to suppress mealybugs sometimes completely. It
tial distribution pattern render the use of many is proved in the case of several mealybugs, par-
insecticides ineffective. Repeated insecticide use, ticularly alien mealybugs. For the biological con-
especially of broad-spectrum chemicals, also trol, a thorough knowledge on mealybugs is
adversely impacts mealybugs natural enemies. highly essential, and identication up to species
Insecticide resistance has also caused the use of is mandatory.
1 Introduction 3

Only very few books are available on Ben-Dov Y (2006) Scales in a family/genus query.
Family pseudococcidae & genus. Available at http://
mealybugs: Mealybugs of California by Accessed
McKenzie (1967), Australian Mealybugs by 14 Aug 2008
Williams (1985), Mealybugs of Central and Charles JG, Cohen D, Walker JTS, Forgie SA, Bell VA,
South America by Williams and Granara de Breen KC (2006) A review of grapevine leafroll asso-
ciated virus type 3 (GLRaV-3) for the New Zealand
Willink (1992), A Systematic Catalogue of the
wine industry. The Horticulture and Food Research
Mealybugs of the World (Insecta, Homoptera, Institute of New Zealand Ltd, Auckland
Coccoidea, Pseudococcidae and Putoidae): With Daane KM, Almeida RPP, Bell VA, Walker JTS,
Data on Geographical Distribution, Host Plants, Botton M, Fallahzadesh M, Mani M, Miano JL,
Sforza R, Walton VM, Zaveizo T (2012) Biology
Biology and Economic Importance by Ben-Dov
and management of mealybugs in vineyards. In:
(1994), and Mealybugs of Southern Asia by Bostman NJ et al (ed) Arthropod management in
Williams (2004). They deal mostly with the taxo- vineyard pests, approaches, and future directions.
nomical aspects of mealybugs in different Springer Science + Media B.V., pp 271307. doi:
regions. Efforts have been made to present infor-
Downie DA, Gullan PJ (2005) Phylogenetic congruence
mation comprehensively about all basic aspects of mealybugs and their primary endosymbionts. J Evol
of mealybugs and also management tactics Biol 18:315324
known for mealybug species affecting different Franco JC, Suma P, da Silva EB, Blumberg D, Mendel Z
(2004) Management strategies of mealybug pests of
crop plants in different countries. Section I of the
citrus in Mediterranean countries. Phytoparasitica
book presents a generalized description of mor- 32:507522
phology, cytogenetics, taxonomy, molecular Kosztarab M, Kozr F (1988) Scale insects of Central
characterization, biology, damage, ecology, natu- Europe. Dr. W. Junk Publishers, Dordrecht
McKenzie HL (1967) Mealybugs of California. University
ral enemies, ant association, control measures,
of California Press, Berkeley, 525 p
insecticide resistance, pheromones, etc. Section Walton VM, Daane KM, Bentley WJ, Millar JG, Larsen
II deals with management practices of mealybugs TE, Malakar-Kuenen R (2006) Pheromone-based mat-
in different crops. ing disruption of Planococcus cus (Hemiptera:
Pseudococcidae) in California vineyards. J Econ
Entomol 99:12801290
Williams DJ (1985) Australian mealybugs. British
References Museum (Natural History), London, 431 p
Williams DJ (2004) Mealybugs of southern Asia. The
Ben-Dov Y (1994) A systematic catalogue of the mealy- Natural History Museum, Southdene Sdn. Bhd., Kaula
bugs of the world (Insecta: Homoptera: Coccoidea: Lumpur, 896 p
Pseudococcidae and Putoidae) with data on geograph- Williams DJ, Granara de Willink MC (1992) Mealybugs
ical distribution, host plants, biology and economic of Central and South America. CAB International,
importance. Intercept Limited, Andover, 686 p Wallingford, 635 p
Part I
M. Mani and C. Shivaraju

Mealybugs are characterised by their bodies mealybug Phenacoccus manihoti Matile-Ferrero

being covered with mealy or wax secretions. has sensory equipment on its antennae that can
They are elongate to oval in shape with distinct detect, by olfaction and contact, chemicals
segmentation (head, thorax and abdomen). released by the plant. Nine different types of sen-
Mealybugs are often characterised as having a silla have been identied on the antenna of the
white, mealy or powdery secretion covering both cassava mealybug. Antennae are remarkable in
dorsal and ventral surfaces of their body. Species Allomyrmococcus Takahashi and other genera of
that occur in concealed habitats such as leaf the tribe Allomyrmococcini, in which they are
sheaths of grasses either lack this secretion or often as long as the body and densely covered in
have only small amounts of it. Marginal areas of slender setae.
their body have a series of protruding lateral wax
laments. These laments may be absent, con- Eyes In certain Pseudococcus species, there are
ned to the posterior one or two abdominal seg- tiny loculi or discoidal pores associated with the
ments, or occur around the entire body margin. A eyes, and these structures appear to have some
lamentous secretion often is produced that taxonomic signicance.
encloses the eggs and at least part of the body.
General morphology of the mealybugs is based Mouthparts The rostrum or beak is a cone-
on common species, and morphological charac- shaped structure that lies approximately between,
ters vary slightly from species to species in and slightly anterior to, the front coxae. As a gen-
mealybugs (McKenzie 1967; Williams 2004). eral rule, the rostrum is approximately one-third
longer than broad, although in some species it is
almost as broad as long. The anterior sclerotised
2.1 Head portion of the mouthpart is the clypeus, including
the internal framework of the tentorium, mandi-
Antennae Antennae are well developed in bles and maxillae bases. The clypeus varies in
adults, normally with ve to nine segments, shape from species to species and may, at times,
except in a few forms where they are reduced to be on taxonomic signicance. The labium
mere two-segmented tubercles. The cassava appears to be three segmented. The basal seg-
ment is quite small and inconspicuous, compris-
M. Mani (*) C. Shivaraju ing a small, sclerotised piece at each side, which
Indian institute of Horticultural Research, constitutes the cone. In mealybugs, there are
Bangalore 560089, India three segments clearly visible on the anterior

Springer India 2016 7

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_2
8 M. Mani and C. Shivaraju

surface of labium. The basal segment usually may be long or short. If they are long, they may
possesses three pairs of setae. At the tip of the extend to or slightly beyond the tip of the claws
apical segment, there is a pair of minute setae that and may be either knobbed or setose at the api-
are usually stiff and spine-like, but because of ces. Digitules less than half the claw length are
their small size they are not shown in the accom- usually setose.
panying illustrations. Immediately anterior to
these apical setae on the anterior surface there are Translucent Dots or Pores They occur on the
usually four pairs of subapical setae. On the hind femur and tibia of quite a few mealybugs.
remainder of the medial and apical segments
there are varying numbers of setae, which reach Clypeolabral Shield In some species, an anterior
their greatest numbers in members of the tribe extension to the clypeolabral shield is present.
Allomyrmococcini associated with herdsmen
ants. There are only two pairs of anterior setae on
the posterior surface of the apical segment in sub- 2.3 Abdomen
family Pseudococcinae, whereas there are three
such pairs of setae in the subfamilies Trabutininae, Dorsal Ostioles The most characteristic feature
Rhizoecinae and Sphaerococcinae. One pair of of the family Pseudococcidae is the occurrence of
the subapical setae is grooved on the labium of two pairs of slit-like openings on the body dor-
Phenacoccus manihoti. sum, here designated as dorsal ostioles. The pos-
terior pair lies within the boundaries of the
seventh abdominal segment, and the anterior pair
appears to belong to the foremost part of the pro-
2.2 Thorax thorax. The edges of the ostioles are invaginated
to form anterior and posterior lips, and these are
Spiracles The spiracles in the Pseudococcidae usually beset with setae and trilocular pores.
are represented by two thoracic pairs only. The When a living mealybug is disturbed or irritated,
anterior pair of spiracles is located in the inter- a globule of liquid is often discharged from one
segmental membrane between the prothorax and or more of these ostioles.
the mesothorax. In the same manner, the poste-
rior pair of spiracles indicates the border between
the mesothorax and the metathorax. In a few spe- Cerarii These structures number at most 18
cies of Antonina and certain other grass-infesting basic pairs. A cerarius is often composed of two
forms, the spiracles are noticeably enlarged, or more conical to lanceolate setae and a compact
sclerotised and often have a conspicuous crescent group of trilocular pores. Each cerarius produces
of crowded trilocular-type pores situated around a lateral wax lament when viewed alive. The
the lateral margin of the atrium. Usually, how- number of cerarii may vary even between species
ever, the spiracles are essentially the same size in the same genus or cerarii may be absent
and shape throughout the family. entirely. Sometimes a cerarius may consist of
only a single conical seta or there may be multi-
Legs A principal leg character was considered ple conical setae. In some species, there are addi-
to be the presence or absence of a denticle or tional, intermediate cerarii present and the cerarii
tooth on the plantar surface of the claw. This may appear to form a continuous row, when it is
tooth has, at its very highest development, a quite difcult to determine the number of basic pairs.
insignicant character, yet it correlates very Usually in the second and third instars, the cerarii
closely with other characters, which in their total- are more clearly dened so that the total number
ity dene the genera that may be referred to as the can be veried. In some cerarii, the conical setae
Phenacoccus series. The claws bear two apically may be replaced by agellate setae surrounded
spatulate or setose digitules that arise, one on by trilocular pores, or a cerarius may contain one
each side, from near the claw bases. The digitules conical seta and one agellate seta. It has been a
2 Morphology 9

Generalised and semidiagramatic drawing representing morphological structure of mealybugs (Courtesy: Williams DJ)
10 M. Mani and C. Shivaraju

custom to refer to the rst three cerarii on the Circulus The circulus when present consists of
head as the frontal, preocular and ocular cerarii. a simple, sclerotised ring enclosing an area of
They are numbered from the anterior end down- variable size. It may be situated on the venter in
wards, as are all body characters. Each of the full the intersegmental fold between the fourth and
complement of cerarii is numbered as C118, with fth abdominal segments, or on the fourth
C1118 occurring on abdominal segments I abdominal segment above. It encloses an area
VIII. The segmentation on the thorax is some- which is free from pores and setae.
times not clearly dened but by tracing the lateral
ends of the intersegmental lines when possible, it Pores and Ducts Several different types of pores
seems that there are two cerarii present on each and ducts on the body may be recognised in the
thoracic segment (C510) and four on the head Pseudococcidae, which include bitubular and trit-
(C14). There are many species with 17 pairs of ubular (sometimes called bi- or tritubular cera res),
cerarii, when C2 (the preocular pair) is missing. trilocular, minute circular (sometimes called sim-
When only a single pair of cerarius is present, it ple disc pores), multilocular (sometimes called
is located on the anal lobes only (C18). Some spe- discoid or genacerores) and quinquelocular types.
cies possess additional, dorsal cerarii.
Trilocular Pores or Swirled Pores They are
Anal Ring The anal ring (anal opening) in the usually present in species of the family
Pseudococcidae is situated on what is here inter- Pseudococcidae. Occasionally, they are larger on
preted as the tenth abdominal segment. The anal the dorsum than on the venter and in some spe-
ring usually lies on the dorsal side of the body situ- cies of Rastrococcus, those in and near the cerarii
ated close to the posterior apex of the abdomen. In are different in shape and size to others elsewhere
some cases, it may be displaced anteriorly on the on the body. Some trilocular pores in Antonina
dorsum and lie some little distance from the poste- and Chaetococcus are as deep as they are wide.
rior apex of the abdomen, and in rare instances it
may be displaced posteriorly to the venter. The Discoidal Pores These are usually minute, sim-
anal opening is usually surrounded by a more or ple, circular pores present in varying numbers over
less sclerotised ring that normally bears six or the dorsum and venter. In some species of
more slender setae. In this sclerotised band in most Dysmicoccus, the discoidal pores have a granular
members of Pseudococcidae appears numerous surface. The rim of each pore may be thin or con-
irregular pores. In a few instances, the ring is much spicuously wide and heavily sclerotised. In the
reduced, the sclerotization is slight and the pores genus Stricklandina, there are normal minute
are absent. pores present and others with thick sclerotised
rims and a granular or tessellated surface.
Anal Lobes The anal lobes are situated on the Occasionally, discoidal pores are oval, as in some
more or less protruding posterior areas of the species of Eurycoccus. In Hordeolicoccus, some
ninth abdominal segment. On the ventral surface, species possess remarkably large discoidal pores,
they possess at the apex usually the longest body each about the same size as a multilocular disc
seta, here designated as anal lobe seta. On the pore. An unusual type of discoidal pore is described
dorsal surface of each anal lobe is a cerarius, herein for some species of Exallomochlus, in
probably more prominent than others along the which the centre of the pore is extended.
body margin because of more trilocular pores,
slender auxiliary setae, two to several stout coni- Tubular Ducts There are many variations in the
cal setae and often a sclerotised dorsal surface. tubular ducts. The presence or absence of oral
rim ducts is sometimes difcult to decide
Vulva The presence of vulva is an indication of because, although the rim may be present, it may
full maturity of the adult female. It is important as not be elevated from the surface of the derm, as in
a landmark to indicate the exact position on the Leptococcus species. Sometimes, oral collar
venter of the anterior margin of the ninth and pos- tubular ducts possess indistinct rims, which are
terior margin of the eighth abdominal segments. discussed in this chapter.
2 Morphology 11

Microducts Structures that appear as minute present with two conical setae in the abdominal
dots on the surface of the cuticle are actually segment IX. Normally, one trilocular disc pore is
microducts. They may be common throughout present in the cerarian zone of each segment.
the Pseudococcidae. Head: Six jointed antennae, average measure-
ments of the segments in are I, 22; II, 21; III,
Ostioles Normally, they are present as two pairs 17; IV, 16; V, 16; VI, 55. Eye is about 15 in
and lie submedially on the dorsum but in the diameter at the base and 7 high. Beak is conical,
Allomyrmococcini they are situated on the lateral on an average 62 long and 40 wide at the
margins, when the sclerotised lips are base. Thorax: Average measurements of posterior
prominent. leg (in ) are as follows: trochanter, 30 19;
femur, 68 27; tibia, 55 18; tarsus, 65 15;
Body Setae Most pseudococcids have at least a claw, 16; tarsal digitule, 23; claw digitule, 15.
few small dorsal setae, and some are quite setose. Both anterior and posterior spiracles are about 6
In certain species the setae are very slender, while in diameter at atrium and about 15 long.
in others they may be stout and conical or lanceo- Abdomen: Anal ring is situated in between two
late, often the same size as that in the cerarii. anal lobes, 26 in diameter; anal ring setae are 44
Rarely the stout setae may be truncated apically, long on an average. Apical setae are 135 long
and at times they may be borne upon a sclerotised on an average. Anal lobe bar is weakly sclero-
process. The setae on the venter are usually slen- tised. Dermal structures: Only one trilocular disc
der, and normally are situated in transverse rows pore is present in each lip of both the anterior and
on the abdominal segments, in a group anterior to the posterior pairs of ostioles. Trilocular disc
the clypeus, and on areas designated as sternal in pores, about 3 , are present in transverse rows on
the thoracic segments. Infrequently the setae are
of taxonomic value at the species level.

Bitubular Cerores and Tritubular

Cerores They are structures peculiar to the sub-
family Rhizoecinae, and in southern Asia they are
present in the genera Rhizoecus and Geococcus.

2.4 Morphology of Various

Instars of Both Sexes
of the Mealybug

Maconellicoccus hirsutus (Green) is taken as

model for detailed descriptions of the nymphs
and adults of both sexes. Seven types of glandular
structure are described, and their roles, mainly in
the production of waxy secretions, are discussed
(Ghose 1971).

2.4.1 First-Instar Nymph

Fig. 2.1 First-instar nymph of M. hirsutus. E eye, AS
At this stage, the male and the female cannot be anterior spiracle, B beak, TDP trilocular disc pore, PS
posterior spiracle, TD tarsal digitule, CD claw digitule,
distinguished. They are elongate to oval, on an
ALB anal lobe bar, APS apical seta, AO anterior ostiole,
average 390 long and 180 wide; anal lobes are PO posterior ostiole, AR anal ring, ARS anal ring seta
prominent (Fig. 2.1). Only one pair of cerarii is (Courtesy: Ghose SK)
12 M. Mani and C. Shivaraju

both dorsum and venter, but more in the former.

Their approximate numbers are dorsal abdominal
segments IX, 4; VIII, 4; VII, 8; VI, 6; V,5; IV, 7;
III, 6; II, 6, metathorax, 10; mesothorax, II; pro-
thorax, 14; head, 10; and ventral abdominal seg-
ments IX, 0; 2 in each of the segments VIII, VII,
VI, V, IV and III; II, 4; metathorax, 5; mesotho-
rax, 4; prothorax, 2; head, 4. The rst instar
nymph differs from other nymphal instars with
the absence of tubular ducts.

2.4.2 Second-Instar Female Nymph

Body is oval with anterior end slightly broader

and rounded; anal lobes are prominent, on an
average 620 long and 360 wide (Fig. 2.2).
Four pairs of cerarii with two conical setae on the Fig. 2.2 Second-instar female nymph of M. hirsutus.
abdominal segments VIIX are present. The cer- CIR circulus, ORD oral rim duct
arian setae of the other abdominal segments are
elongated and slender. Usually, two ducts of oral
rim type and three trilocular disc pores in each mesothorax, 35; prothorax, 40; head, 20; and
cerarian zone of segments IX and VIII and two ventral abdominal segments IX, 4; VIII, 2; VII,
disc pores in the ceracian zone of all other 4; VI, 6; V, 4; IV, 6; Ill, 4; II, 5; metathorax, 9;
abdominal segments are present. Head: Six mesothorax, 14; prothorax, 15; head, 5. Tubular
jointed antennae, average measurements in are ducts of oral rim type about 8 long and 5 wide
I, 35; II, 23; III, 33; IV, 21; V, 21; VI, 62. Eye are present on dorsum. Their numbers are abdom-
about 21 in diameter at the base and 9 high. inal segments IX, 2; VIII, 2; VII, 0; VI, 3; V, 4:
Beak is conical, on an average 83 long and 52 IV, 4; III, 5; II, 4; metathorax, 6; mesothorax, 7;
wide at the base. Thorax: Average measurements prothorax, 10; head, 3. Only one duct is present
of posterior leg in are trochanter, 42 24; in the venter of abdominal segment VIII.
femur, 85 35; tibia, 70 23; tarsus, 70 l8;
claw, 21; tarsal digitule, 34; claw digitule, 19.
Anterior spiracle is about 29 long and 10 2.4.3 Third-Instar Female Nymph
wide at atrium; posterior one is about 32 long
and 10 at atrium. Abdomen: Anal ring 41 in Body is oval with anterior end slightly broader
diameter; anal ring setae 64 long on an average. and rounded; anal lobes are prominent, on an
Apical setae 173 long on an average. A moder- average 1.095 mm long and 0.678 mm wide. Five
ately sclerotised bar is present in each anal lobe. pairs of cerarii are present on the last ve abdom-
Circulus is present. Dermal structures: Anterior inal segments, usually with two conical setae in
pair of ostioles with two trilocular disc pores and each. Anal lobe cerarii each with three trilocular
one seta on each lip; posterior ones each with disc pores and one oral rim duct and the remain-
three pores and one seta on the upper lip and two ing each cerarius with two disc pores and one
pores on the lower lip. Trilocular disc pores are oral rim duct are present. Head: Seven jointed
present on both dorsum and venter. Dorsal pores antennae, average measurements in are I, 45; II,
measure 4.04.4 and ventral ones 3.23.6 39; III, 31; IV, 26; V, 27; VI, 30; VII, 74. Eye is
wide. Their approximate numbers are dorsal about 25 in diameter at the base and 15 high.
abdominal segments IX, 6; VIII, 9; VII, 15; VI, Beak is conical, on an average 98 long and 52
II; V, 12: IV, 12; III, 10; II, 10; metathorax, 20; wide at the base. Thorax: Average measurements
2 Morphology 13

of posterior leg in are trochanter, 66 34; rax, 23; mesothorax, 36; prothorax, 42; head, 20;
femur, 127 53; tibia, 121 30; tarsus, 87 26; and ventral abdominal segments IX, 4; VIII, 11;
claw, 27; tarsal digitule, 36; claw digitule, 24. VII, 12; VI, 13; V, 10; IV, 10; III, 12; II, 12; meta-
Anterior spiracle is about 34 long and 13 thorax, 15; mesothorax, 28; prothorax, 24; head,
wide at atrium; posterior one is 36 long and 13 13. Tubular ducts of oral rim type are present
wide. Abdomen: Anal lobes are prominent; anal mostly on dorsum and a few on venter. Ducts on
ring on an average is 60 in diameter; anal ring dorsum are 9 long and 6 wide. Ventral ducts
setae are 84 long; apical setae is 209 long on are about 3/4 wide of those in dorsum. Their
an average. Anal lobe bar is moderately sclero- approximate numbers are dorsal abdominal seg-
tised. Dermal structures: Ostioles can be found ments IX, 6; VIII, 11; VII, 4; VI, 10; V, 11; IV, 14;
with a few trilocular disc pores. Anterior pair III, 14; II, 14; metathorax, 21; mesothorax, 27;
with three pores and one seta on each lip; poste- prothorax, 19; head, 7; and ventral abdominal seg-
rior ones with three to four pores and zero to one ments IX, 0; VIII, 2; VII, 2; VI, 2; V, 2; IV, 2; III,
seta on each lip. Dorsal setae are of two sizes, 3; II, 3; metathorax, 2; mesothorax, 6; prothorax,
longer and stout, and shorter and thin. Ventral 6; head, 4. Tubular ducts are of oral collar type,
body setae are longer and agellate. Circulus is 3.54.0 long and 1.5 wide, mostly distributed
about 33 long. Trilocular disc pores, 3.23.6 , in the marginal and submarginal areas of venter,
are present on both the surfaces of the body but rarely found on dorsum. Their approximate num-
more on dorsum. Their approximate numbers are bers in venter are abdominal segments IX, 0; VIII,
dorsal abdominal segments IX, 14; VIII, 15; VII, 2; VII, 4; VI, 5; V, 4; IV, 4; III, 4; II, 7; metathorax,
32; VI, 19; V, 18; IV, 19; III, 30; II, 30; metatho- 10; mesothorax, 8; prothorax, 4; head, 4.

Third-instar female nymph of M. hirsutus (Green). Adult female of M. hirsutus. MLDP multilocular disc
OCD oral collar duct, ORD oral rim duct pore, VUL vulva
(Courtesy: Ghose SK)
14 M. Mani and C. Shivaraju

2.4.4 Adult Female former being predominant in the dorsum and the
latter in the venter. Oral rim ducts of dorsum are
Body is ovoid, slightly broader and rounded at larger than those of venter and more or less
the anterior end, on an average 1.7 mm long and arranged in transverse rows, about 9.5 long and
1.1 mm wide, attaining larger size (3.2 mm l.7 45 in diameter at the opening. Their approxi-
mm) with maturity. Anal lobes are prominent, mate numbers are abdominal segments IX, 12;
particularly in young adults. Six pairs of cerarii VIII, 20; VII, 10; VI, 22; V, 32; VI, 35; III, 34;
in the abdominal segments IVIX, usually with I1, 36; metathorax, 54; mesothorax, 62; protho-
two cerarian setae are present; occasionally a rax, 42; head, 18. A few rim ducts of venter are
third one is present in the cerarii of segments VIII found in the marginal and submarginal regions of
and IX. Segment IV has generally only one cerar- the body. Their numbers are abdominal segments
ian and one stout and longer setae on one side, IX, 2; VIII, 4; VII, 3; VI, 5; V, 5; IV, 7; III, 7; II,
the other cerarius has two normal cerarian setae. 6; rnetathorax, 4; mesothorax, 7; prothorax, 8;
Cerarii are without auxiliary setae except the anal head, 4. Oral collar ducts of venter are variable in
lobe pair. Each cerarius of segment IX has 56 size, 2.42.8 in diameter at opening and on an
trilobular disc pores and three oral rim ducts. average 10.5 long. The ducts of the dorsum are
Head: Antennae appear to be nine jointed generally smaller. These ducts are much more
because of a pseudo-articulation in the terminal numerous (six to seven times) in the adult than in
joint. Average measurements in are I, 54; II, 54; the third nymphal female. Multilocular disc
III, 52; IV, 34; V, 41; VI, 40; VII, 39; VIII, pores, 5 in diameter, are restricted to the sub-
37 + 56. Eye is about 32 wide at the base and 22 marginal and median regions of venter, mainly in
high. Beak is conical, on an average 141 long the abdominal segments VIIX.
and 86 wide at the base.
Thorax: Average measurements of posterior
leg in are trochanter, 97 36; femur, 217 68; 2.4.5 Second-Instar Male Nymph
tibia, 227 32; tarsus, 100 27; claw, 33; tarsal
digitule, 49; claw digitule, 31. Tarsal digitule, of Body is oval with anterior end slightly broader
the anterior legs are unequal, one is about 49 , and rounded; anal lobes are prominent. Average
whereas the other is about 42 . Anterior spiracle body size in the early stage is 625 long and 390
is about 51 long and 26 wide at atrium, and wide. It increases greatly and attains 970 438
posterior one 55 long and 29 wide. at the end of the feeding period. Normally, one
Abdomen: Anal ring on an average is 72 in pair of cerarii present are in the abdominal seg-
diameter; anal ring setae is 154 long; anal lobe ment IX; generally each with two and rarely stout
bar is moderately sclerotised; apical setae are 251 conical setae, one auxiliary seta, one microduct of
on an average. Dermal structures: Anterior pair oral collar type and one trilocular disc pore.
of ostioles with nine to ten trilocular disc pores Segment VIII is occasionally with one or two cer-
and one to three setae on each lip are present; arian setae in each. The cerarian setae of other
posterior one with 912 pores and 14 setae on segments are slender and elongated. Generally,
each lip. Body setae are of two sizes on both dor- two disc pores and one collar duct are present in
sal and ventral surfaces, the ventral ones being each cerarian zone of other segments. Head: Six
generally longer. Circulus is about 77 long. jointed antennae, but the joints cannot be recog-
Trilocular disc pores are more numerous and nised as and when the antennae of third-instar
larger on dorsum, about 4 , whereas those on male nymphs develop inside this instar. Average
venter measure about 3 . These pores are much measurements of the segments in are I, 32; 11,
more numerous (above 20 %) in the adult than in 27; III, 34; IV, 20; V, 22; VI, 62. Eye is about 22
the third-instar females. Tubular ducts are of two in diameter at the base and 10 high. Beak is
types: oral rim ducts and oral collar ducts, the conical, on an average 94 long and 57 wide at
2 Morphology 15

the base. Thorax: Average measurements of pos- imate numbers are dorsal abdominal segments IX,
terior leg in are trochanter, 46 26; femur, 9; VIII, 9; VII, 18; VI, 13; V, 15; IV, 16; III, 22; II,
98 38; tibia, 84 20; tarsus, 74 18; claw, 21; 19; metathorax, 20; mesothorax, 44; prothorax,
tarsal digitule, 34; claw digitule, 20. Anterior spir- 32; head, 26; and ventral abdominal segments IX,
acle is about 29 long and 8 wide at atrium; 4; VIII, 5; VII, 10; VI, 9; V, 8; IV, 7; III, 8; II, 7;
posterior one about 31 long and 9 at atrium. metathorax, 11; mesothorax, 21; prothorax, 16;
Abdomen: Anal ring on an average is 36 in head, 17. The microducts are of oral collar type,
diameter; anal ring setae are 66 long; apical about 7 long, present on both dorsum and ven-
setae are on an average 172 long. Anal lobe bar ter. The ducts in dorsum are wider (3.23.6 )
is moderately sclerotised. Dermal structures: than those in venter about 2.4 ; their numbers are
Three trilocular disc pores and one to three setae dorsal abdominal segments IX, 2; VIII, 5; VII, 2;
on both upper and lower lips of anterior pair of VI, 2; V, 2; IV, 5; III, 3; II, 7; metathorax, 4; meso-
ostioles and two to three pores and zero to one thorax, 6; prothorax, 5; head, 4; and ventral
seta on each lip of the posterior pair are present. abdominal segments IX, 0; VIII, 1; VII, 3; VI, 4;
Circulus is present. Trilocular disc pores are about V, 3; IV, 2; III, 2; II, 2; metathorax, 2; mesothorax,
3 and more numerous on dorsum. Their approx- 2; prothorax, 2; head, 3.

Second-instar male nymph of M. hirsulus. OCD oral Third-instar male nymph of M. hirsutus. ANT antenna, AS
collar duct anterior spiracle, MLDP multilocular disc pore, AO ante-
(Courtesy: Ghose SK) rior ostiole, PO posterior ostiole, AT anal tube, WL

2.4.6 Third-Instar Male Nymph the antennae of fourth-instar male become prom-
inent, as and when these are formed inside the
Body is oval, more rounded at the anterior end, antennae of third instar. Mouthparts are absent.
on an average 1.138 mm long and 0.504 mm Eyes are not discernible.
wide. Sclerotisation is in general very weak. Thorax: Two small wing buds more or less at
Head: Segmentation of antennae is obscure, right angles to the lateral margins of the mesotho-
with the average length being 276 . The joints of rax. Legs are short in comparison with body
16 M. Mani and C. Shivaraju

length, with a few pointed setae. Average mea- present in between the abdominal segments
surements in are trochanter, 52 32; femur, IXX, but its opening on dorsum or venter is not
112 43; segmentation of tibia, tarsus and claw is discernible. Near the posterior end of the abdo-
not well differentiated, their combined length and men, six to seven setae are arranged transversely.
maximum breadth being 175 31. Tarsal and Marginal and submarginal areas of segment IX
claw digitules are absent. Anterior spiracle is dorsally with ve to six more or less transversely
about 29 and posterior one is 29 long and 14 arranged setae are present.
wide. Dermal structures: Both anterior and posterior
Abdomen: Anal ring is absent. A well- pair of ostioles are present. Trilocular disc pores
sclerotised anal tube, 23 long and 26 wide, is are absent.

Fourth-instar male nymph of M. hirsutus. WP wing pad Adult male of M. hirsutus. CS coronal suture, DS
Digitiform seta, QDP quadrilocular disc pore, PS penial
sheath, PW part of wing, PSG penta locular stellate gland,
DE dorsal eye, LE lateral eye, VE ventral eye
2 Morphology 17

Multilocular disc pores: It is 5 in diameter, Dermal structures: Both anterior and posterior
found on both dorsum and venter. Their numbers pairs of ostioles are present, with two multilocu-
are dorsal abdominal segments IX, 1; VIII, 4; lar disc pores and one seta on each lip of posterior
VII, 11; VI, 3; V, 4; IV, 4; III, 9; II, 4; metathorax, pair. Multilocular disc pores, 5 in diameter, are
2; mesothorax, 6; prothorax, 13; head, 8; and present on both dorsum and venter. Their num-
ventral abdominal segments IX, 0; VIII, 2; VII, 3; bers are dorsal abdominal segments IX, 0; VIII,
VI, 3; V, 3; IV, 4; III, 2; II, 2; metathorax, 8; 3; VII, 9; VI, 3; V, 4; IV, 4; III, 4; II, 4; metatho-
mesothorax, 7; prothorax, 6; head 0. Microducts rax, 5; mesothorax, 3; prothorax, 12; head, 0; and
are of oral collar type, about long, present on ventral abdominal segments, IX, 0; VIII, 2; VII,
both dorsum and venter. Ducts of dorsum are 2; VI, 2; V, 2; IV, 3; III, 2; II, 4; metathorax, 5;
about 3.2 wide, whereas those of venter are mesothorax, 5; prothorax, 4; head, 0. Microducts
about 2.4 . Their numbers are dorsal abdominal are of oral collar type, about 7 long, present on
segments IX, 0; VIII, 7; VII, 5; VI, 10; V, 10; IV, both dorsum and venter. The ducts of dorsum are
14; III, 19; II, 19; metathorax, 14; mesothorax, 4; much wider (about 3.2 ) than those of venter
prothorax, 16; head, 4; and ventral abdominal (1.82.4 ) arranged more or less in transverse
segments IX, 0; VI, 3; VII, 4; VI, 7; V, 5; IV, 5; rows. Their approximate numbers are dorsal
III, 8; II, 4; metathorax, 5; mesothorax, 2; protho- abdominal segments IX, 0; VIII, 13; VII, 10; VI,
rax, 6: head, 3. 13; V, 13; IV, 17; III, 17; II, 11; metathorax, 8;
mesothorax, 4; prothorax, 30; head, 4; and ven-
tral abdominal segments IX, 0; VIII, 4; VII, 8; VI,
2.4.7 Fourth-Instar Male Nymph 8; V, 8; IV, 12; III, 01; II, 0; metathorax, 0;
mesothorax, 0; prothorax, 10; head, 0.
Anterior end of the body is round, narrowing Adult males are only of macropterous form,
gradually on the posterior end, on an average on an average 1.055 mm long, including the pro-
1.061 mm long and 0.340 mm wide. Head, thorax jected penial sheath, and 0.310 mm wide. Head:
and abdomen are more differentiated than the Ten jointed antennae, average measurements in
previous instar; sclerotisation is weak. Head: Ten are I, 39; II, 66; III, 79; IV, 69; V, 66; VI, 63; VII,
jointed antennae, average measurements in are 67; VIII, 67; IX, 58; X, 71. The antennae are
I, 34; II, 46; III, 34; IV, 24; V, 27; VI, 29; VII, 32; clothed mainly with digtiform setae, up to about
VIII, 37; IX, 34; X, 74; second segment is the 39 ; a few thicker specialised digtiform setae are
broadest. Mouthparts are absent. Eyes are not present on the last three apical segments, the lon-
discernible. Thorax: Average measurements of gest ones being 39, 49 and 49 on segments VIII,
hind leg in are trochanter; 60 29; femur, IX and X, respectively. Coronal suture is well
128 44; tibia, 142 28; tarsus, 101 25; claw, developed. Dorsomedian sclerite is weakly
16; tarsal and claw digitules are absent. Anterior sclerotised. Three pairs of eyes are present: dor-
spiracle is about 26 long and 13 wide at sal, ventral and lateral. The average diameter of
atrium; posterior one is about 31 long and 16 the dorsal and ventral pairs is 30 and 34 , respec-
at atrium. Wing pads are obliquely attached to tively. Lateral pair is 25 in diameter at the base
the mesothorax. Abdomen: In segment X, six to and 18 high on an average. Mouthparts are
seven setae are transversely arranged on dorsum. absent. Thorax: One pair of wings, on an average
Two marginal setae are on dorsum on each side 0.92 mm long and 0 .42 mm wide; each wing has
of segment IX, the longest one about 63 , and four to ve sensory setae near the basal region;
two corresponding ones on venter about 17 . average measurements of the posterior leg in
Anal tube, apparently without an external open- are trochanter, 62 26; femur, 216 39; tibia,
ing, is present in between segments IX and X, 22 283 23; tarsus, 99 19; claw, 34; tarsal digitule
long and 26 wide. Penial sheath of adult male is very slender, 34. As in antennae, legs are
is visible as and when it is formed inside this clothed with both digitiform and slender-pointed
stage. setae, their maximum length being 31 and 21 ,
18 M. Mani and C. Shivaraju

respectively. The inner distal end of tibia has disc pores are present on each side of the
three spines. Tarsus has three to four spines at the abdominal segment IX. In the centre of each clus-
inner distal end. Anterior and posterior spiracles ter, there are eight to ten disc pores of smaller
are about 21 wide at atrium, their lengths being dimension (about 4 in diameter) and three long
23 and 26 . Abdomen: Penial sheath is about 179 setae, two of which on an average are 260 long.
long and 70 at the widest portion and 6.5 at Around the central zone 3844 disc pores, 5 in
the projected tip, which is rounded. It has two diameter, are present.
distinct median lobes, each more or less triangu-
lar in shape. Dermal structures: Only posterior
pair of ostioles is present. Quadrilocular disc References
pores, 4.85.6 in diameter, are present on both
dorsum and venter; numbers on dorsum are Ghose SK (1971) Morphology of various instars of both
sexes of the mealy-bug, Maconellicoccus hirsutus
abdominal segments IX, 0; VIII, 4; VII, 2; VI, 2;
(Green) (Pseudococcidae: Hemiptera). Indian J Agric
V, 3; IV, 2; III, 2; II, 11; metathorax, 0; mesotho- Sci 41(7):602611
rax, 0; prothorax, 816; head, 4; and ventral McKenzie HL (1967) Morphology and classication.
abdominal segments IX, 0; VIII, 3; VII, 3; VI, 3; Mealybugs of California, University of California
Press, Berkeley, pp 3640
V, 3; IV, 3; III, 0; II, 2; metathorax, 2; mesotho-
Williams DJ (2004) Mealybugs of southern Asia. The
rax, 48; prothorax, 48; head, 0. Two dorsal Natural History Museum, Southdene Sdn. Bhd., Kaula
clusters of stellate or tail-forming pentalocular Lumpur, Malaysia, pp 1821
Ramakrishna Sompalaym, Kokilamani A.
Lingarajaiah, Raju G. Narayanappa, Jayaprakash,
and Venkatachalaiah Govindaiah

3.1 Introduction Schraders interpretation was later conrmed

experimentally with a mealybug, for example,
The coccoids which include mealybugs are a rel- Pseudococcus obscurus and/or Planococcus citri
atively small group of highly specialized hemip- by Brown and his associates (Brown 1958, 1959,
teran insects. They are parasitic on plants and 1963, 1964, 1965, 1969; Brown and Nelson-Rees
quite sedentary in behavior (Miller and Kosztarab 1961; Chandra 1962, 1963a, b; Brown and Nur
1979; Gullan and Kosztarab 1997; Mani 1989; 1964; Baer 1965; Nur 1963, 1966a, b, 1967;
Kondo et al. 2008). The chromosome system of Brown and Weigmann 1969). Earlier cytological
coccoids is of special interest because it is char- scrutiny had been reviewed by White (1973) and
acterized by chromosomal heterochromatization certain aspects of coccoid chromosome systems
or elimination of the paternal endowment of especially their possible role in the involvement
chromosomes during early embryogeny of the in the chromosome imprinting processes, have
male in the majority of scale insects. The rst been aptly dealt with by Brown (1977) and
cytological insight into the nature of this remark- Brown and Chandra (1977), about certain unusual
able system came from the pioneering cytology features by Nur (1980, 1990), and about recent
described by Schrader (1921, 1923a). Subsequent achievements made with respect to biochemical-
studies by Hughes-Schrader (1948) have pro- based cytology by Prantera and Bongiorni (2012).
vided insightful thoughts into the explanation of Enormous and extensive cytological and genetic
the genetic and evolutionary implications of studies of mealybugs belonging to worldwide fauna
paternal heterochromatization that could serve are available (Little 1957; Carter 1962). However,
as an intermediate stage between regular diploidy the efforts on the systematic and cytogenetic aspects
and true male-haploidy. of Indian coccoids are very limited. There have

Department of Zoology, Bangalore University,
R. Sompalaym (*) K.A. Lingarajaiah
Bengaluru 560 056, India
Department of Zoology, Bangalore University,
Bengaluru 560 056, India Centre for Applied Genetics, Bangalore University,
e-mail: Bengaluru 560 056, India
R.G. Narayanappa V. Govindaiah
Department of Biotechnology, KSOU, Centre for Applied Genetics, Bangalore University,
Mukthagangotri, Mysore 570 006, India Bengaluru 560 056, India

Springer India 2016 19

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_3
20 R. Sompalaym et al.

been sporadic reports that provide incomplete and during successive divisions. In the absence of
contradictory information pertaining to Indian kinetochore-based cell divisions that prevail in
fauna for their chromosome systems (Tulsyan coccoid chromosome systems, and also, in order
1963; Dikshith 1964, 1966; Chauhan 1970, 1977). to accommodate the occurrence of karyotypic
changes, Brown (1961) assays chromosome frac-
ture and fusions in the place of the prevalent
3.2 Mealybug Chromosomes nature of chromosomal rearrangements. It was
also envisaged that simple breakage can deter-
All coccoids possess holocentric chromosomes, mine increase or decrease in chromosome num-
that is, diffuse centromeres (Hughes-Schrader bers unless a breakagefusionbridge cycle
and Ris 1941). Inverse meiosis is a second ances- intervenes to eliminate the breakage points.
tral condition manifested in coccoids that is also Species relationships can be explained by cit-
shared with the other closely allied aphids (Ris ing chromosome variability occurring with
1942; Hughes-Schrader 1944, 1948). respect to either chromosome numbers or mor-
Although the cell cycle sequence is different phology. Brown (1961) insists upon spontaneous
from that of typical meiosis, results are the same; occurrence of chromosome breakage resulting in
each of the four chromatids of meiotic bivalents abundant availability of ruptured chromosomes
reaches one of the four nuclei produced by meio- for increase in the diploid numbers either by
sis. Coccoids are also manifested by those systems chance or incurred by selection. There are an
in which at least some of the females are produced abundant number of cases dealing with karyo-
parthenogenetically, in addition to the usual bisex- typic changes incurring based on chromosome
ual mode of reproduction. They are considered to fragmentation in mealybug genomes (Nur et al.
have unique chromosome systems and they offer 1987; Cook 2000).
enormous potential in our understanding of prob- Changes in chromosome numbers with respect
lems such as chromosome imprinting and differ- to pseudococcid species have been reported to be
ential regulation of homologous chromosome sets in the range of 8 to 64 and that ranges within coc-
(Chandra 1971; Chandra and Brown 1973). coids are rather small compared to other insect
Chandra (1971) suggested for the rst time that groups (Hughes-Schrader 1948; Nur et al. 1987).
there are some similarities and also contrasts Until now, 115 cytogenetically studied species of
between mammalian X-chromosome inactivation mealybugs belonging to 44 genera have been
and the inactivation of paternal chromosomes in made known (Gavrilov 2007; Gavrilov and
mealybugs. These include genomic imprinting, Trapeznikova 2007, 2010). Eventhough, the dip-
facultative heterochromatization, and differential loid number of chromosomes ranges from 8 to 64,
regulation of homologous chromosomes. the modal number seem to fall on 10 (Plate 3.6
Subsequently, Brown and Chandra (1977) have Fig. 4, 6, 8). Few mealybugs showed intrageneric
drawn attention to emphasize that coccoids are at variation in their chromosome numbers; for exam-
the pinnacle of an evolutionary pyramid of cytoge- ple, in genera such as Antonina (2n = 12, 16,
netic variants and complexity. In order to under- 24 + Bs), Nesopedronia (2n = 18, 14, 10) and
stand these variations in chromosome mechanics, Trionymus (2n = 16, 10, 8), such instances can be
it becomes essential briey to review pseudococ- cited as useful in taxonomic and phylogenetic con-
cid chromosomes. siderations of the genus. Accessory chromosomal
elements (B-chromosomes) were found in several
species of mealybugs (Nur et al. 1987; Gavrilov
3.3 Chromosome Numbers 2004). But, the detailed investigation of
and Chromosome Forms B-chromosomes has been done only in
Pseudococcus viburni (Signoret; Nur 1962a,
Coccoid chromosomes lack specied centro- 1966a, b). The majority of pseudococcids possess
meric regions. It appears obvious to point out that 2n = 10 (Nur et al. 1987; Moharana 1990; Nur
chromosome fragments perpetuate themselves 1990; Gavrilov and Trapeznikova 2007, 2010).
3 Cytogenetics 21

Excepting Planococcus citri and a few other spe- species. Based upon female pachytene chromo-
cies, the number of species studied based on meric sequences, Raju (1994) made an initial
employing recently evolved cytogenetic tech- attempt to describe karyotype and comparison of
niques is very low. One of the reasons cited was three species of the Indian genus Planococcus
the difculties incurred in procuring enough cells (viz. P. citri, P. lilacinus and P. pacicus) essen-
for the preparation of chromosomes and of under- tially based on differential banding patterns, but
standing of chromosome basics for detailed cyto- was unable to identify individualistic karyotypes
logical analyses. For cytological investigations of because of lack of discriminating cytogenetic fea-
Indian mealybug taxa, Parida and Moharana tures (Plates 15). Gavrilov (2004a, 2007) and
(1982) and Moharana (1990) attempted to enu- Gavrilov and Trapeznikova (2007, 2010) have
merate chromosome numbers based on conven- made elaborate studies resulting in the elucidation
tional cytological techniques and they were also of the karyotype for more than 25 species of
able to present preliminary assessments of karyo- Russian mealybugs based on squashing techniques
morphological features for more than 20 different for chromosomal preparations. Nur et al. (1987)

Plate 3.1 Planococcus citri

22 R. Sompalaym et al.

Plate 3.2 Planococcus lilacinus

were able to describe the karyotype of about 80 Mckenzie 1967 (California), Drozdovskiy 1966
different species of mealybugs that were collected (Russia), Brown 1961 and Hughes-Schrader 1935
from various parts of Africa, America, and a few (USA), and Schrader 1923a (USA) have contributed
from South Asia. Tremblay et al. 1977 (Italy), enormously to the eld of mealybug cytogenetics
3 Cytogenetics 23

Plate 3.3 Planococcus pacicus

in the form of karyological studies. In an attempt complements did not provide any discriminative
to analyse mealybug chromosome morphology, cytological signatures other than suggesting that
chromosome preparations were studied through they belong to and qualify themselves as belong-
the uorescent microscopy using appropriate dyes ing to the Lecanoid type of chromosome system
(e.g., Quinacrine Mustard (QM)/QM dihydrochlo- (Jaipuriar et al. 1985; Venkatachalaiah and
ride), and it was found that these chromosomal Chowdaiah 1987; Venkatachalaiah 1989).
24 R. Sompalaym et al.

Plate 3.4 Planococcus pacicus

3.4 Telomeres and C- Bands C-staining proles along the length of each chro-
mosomal fragment in the complement.
It is of interest to note that with particular impor- Employing classical C-staining protocol upon
tance to the diffuse nature of centromeric systems Planococcus citri metaphase chromosomal prep-
manifested by coccoid chromosome morphology arations, it was expected to highlight constitu-
it was expected to display discriminative tively heterochromatic sites in the complement.
3 Cytogenetics 25

Plate 3.5 Planococcus citri

26 R. Sompalaym et al.

Plate 3.6 Representatives of other pseudococcids

But the cursory observations led in demonstrat- this chromosomal component may offer convey-
ing that the C-specic bands were found speci- ing information about its cytogenetic context.
cally identifying the telomeric region specicity The situation acquires a genetic signature due to
in the metaphasic chromosomal complement and its co-orientation pairings during late meiotic
this situation was ascribed as T-bands (male or female) chromosome synaptic processes
(Venkatachalaiah 1989; Raju 1994). However, (Plate 3.7 Fig. 6, 7, 8, 9).
the results obtained by Venkatachalaiah (1989) Ferraro et al. (1998), in their attempt to local-
and Raju (1994) pertaining to C-banded stainings ize C-banded regions at P. citri chromosomal
at telomeric ends of each chromosome in the preparations, found evidence regarding
complement were irrespective of a particular C-positive bands localizing at the telomeric
chromosome type (whether of mitotic, meiotic, regions of all chromosomes in the complement.
or polyploid nuclei) or sexes (males or females), When they further insisted upon prior exposure
and thus, they contend that these cytological to CMA3 (chromomycin A3) -methyl green and
markers could be representing a particular type subsequent exposure to C-staining protocols, the
of constitutive heterochromatic component. The implicit C-bands were found correspond to telo-
intense stainability at the telomeric regions in the meric region-specic areas. This has led them to
chromosomal content allows one to assay that infer that these results could, however, representing
3 Cytogenetics 27

Plate 3.7 Representatives of other pseudococcids showing NOR- entities and C-band regions

GC-rich specic spots on chromosomes. From the point of view of cytology, telomeres
However, when they insisted further upon are marked by specialized DNA and protein
H33258 uorochrome to live cells prior to components that usually decorate the chromo-
C-staining, they recovered images almost imitat- some ends or other specic loci. In several
ing C-banded telomeric-specic regions. Thus eukaryotes, their occurrence and prevalence has
they were able to interpret the failure to nd a been tested, wherein they have been found com-
dull appearance, instead of bright bands at the posed of simple tandem pentameric (TTAGG)
specied locales, and those of brighter and repeats localizable at specic chromosome loci
intense bandings could represent condensed con- accompanied by complex subtelomeric struc-
stitutive heterochromatic regions, leading them tures in close apposition (DAiuto et al. 2003; De
to insist that there could be more DNA congre- Lange 2005). A large number of molecular cyto-
gated per unit length per chromosome than in the logical studies have led to the implication that
euchromatic zones. Moreover, some of the telo- telomeres of eukaryotes are usually composed of
meric regions being positive to DAPI stainings, it conserved short tandemly repeated GC-rich
was inferred that the presence of AT-rich sequences. This kind of sequence conservation is
sequences were embedded within the predomi- reected as a common mechanism for telomere
nantly GC-rich regions of individual region biosynthesis. This mechanism specically
chromosomes. dictates and involves the activity pattern of a
28 R. Sompalaym et al.

telomerase, a ribonucleoprotein DNA poly- tion of TTAGG repeats decorating at chromo-

merase enzyme that compensates any further loss somal interstitial regions. Because of their
of terminal sequences at every replication round resistance to higher doses of ionizing radiation, a
by adding short tandem GC-rich sequences onto unique feature characterizing the mealybug
the chromosome ends (Greider 1995). genome and this extraordinary chromosomal
Studies in various insect species demonstrated phenomena could as well serve as an asset
characteristic presence towards the notion that towards relegating them to be considered as a
TTAGG repeats are an ancient motif traceable in radiation-resistant coccid.
Arthropoda and that those pentameric TTAGG Mohan et al. (2012) further attempted to test
repeats that could have been originated from the responses with still higher doses of ionizing radia-
vertebrate TTAGGG hexamers (Frydrychov tion exposure on P. citri genomes and were thus
et al. 2004; Vitkova et al. 2005). able to utilize this opportunity to suggest that
Cytogenetic scrutiny undertaken by Mohan mealybug genome may well serve as a unique
et al. (2011) with regard to Planococcus citri genetic system. The results of their explorations
chromosomes have enabled them to delineate the revealed that especially pounding concentration
presence of a characteristic pattern of telomeric on the centromeric property that was eventually
sequences and also some of their placements recognized as sites of activity sporadically spread-
upon the respective interstitial loci and the con- ing over the length, and in spite of this enormity
stitutive presence of active telomerases was there is no signicant loss of the genetic material.
detected and this was achieved by introducing Furthermore, with respect to the mealybug
single primer PCR and Southern hybridization genome, it was considered to contain highly toler-
protocols upon cytological preparations. The able radiation doses as high as 1100 Gy. Presently,
results so obtained suggest that in particular, P. it is apparent that mealybug genomes may serve as
citri chromosome complement seemed to pro- very efcient agents of the DNA repair machinery
vide as an efcient chromosome marker to system that ensures proper healing of double-
demarcate the chromosomal loci at the site of the strand breaks (dsb) invaded by ionizing radiation.
mechanism of formulation of TTAGG repeats at Despite several special qualities,proclaimed as
their respective chromosome ends. In addition, containing, for example, of telomeric repeats
this study was also aided in identifying and thus along with interstitial sites of chromosomes and
disclosing whether some unrelated low copy with respect to maintenance and sustainability of
repeats, called Intercept TTAGG Sequences telomeres to higher radiation effects, some authors
(ITS) were displaying identiable spots based on believe regardless of the vulnerability of the telo-
their presence, thereby intercepting the repetitive meric-independent mechanism it could also be
elements. It is well known that P. citri genomes operating in a P. citri genetic system.
are bestowed with diffuse centromere (holocen- Thus, the occurrence of C-heterochromatin
tric) activity and as a consequence of this nature occupying telomeric regions of chromosomes
there could be an obvious presence of multiple deserves some comments. In its usual courses of
centromeric zones occupying the length along other cases, incidentally pertaining to holocentric
individual chromosomes. Utilizing this extraor- chromosome systems, it was possible to ascribe
dinary condition, in view of these genetic pecu- that C-heterochromatin is preferentially located
liarities persisted with elegant DNA repair at or near telomeres (Muramoto 1980; Camacho
machinery that ensures the protection of addi- et al. 1985; Papeschi 1998; Panzera et al. 1992).
tional chromosomal elements localizing at inter- According to Heitzs (1933) equilocal hetero-
stitial zones; and thus they aptly recognize these chromatin distribution hypothesis, it was
sites as putative zones. Surprisingly, following inferred that the C-banding material in both
X-ray irradiation upon these broken chromo- homologous and nonhomologous chromosomal
somal ends it was disclosed that some loci were sets tends to congregate at homogeneous and
characteristic and were tagged with the associa- homologous regions, thereby occupying similar
3 Cytogenetics 29

kinds of cytological sites, and thus probably rep- (Nucleolar Organizer Region) specicities on
resented by either telomeric and/or centromeric metaphase chromosomes. These results point to
sequences. Schweizer and Loidl (1987) have pro- have driven them to ascribe that the FISH tech-
posed a model that explains how nique might help in identify with P. citri chromo-
C-heterochromatin enhances and leads to adher- somes at specic zones on all chromosomes
ence of such chromosomal zones conning and/ except at one pair in the complement. But silver
or inducing towards effecting interchanges of nitrate staining specicity had enabled in speci-
heterochromatic material between nonhomolo- fying at a single pair in the complement but char-
gous and homologous chromosomes in the com- acteristically demonstrating the site at which
plement and thus leading towards annealing into bearing very prominent macer-shaped, silver
a common platform resulting in such situation nitrate stainable entities, irrespective of their ori-
that they belong to as though in a monocentric gin whether of euchromatic or heterochromatic
type of chromosome system; that also insists chromosomal pair (Plate 3.7 Fig. 1, 2, 3, 4, 5).
upon those of chromosomal regions with holoki-
netic activity that do not t into this model. In
view of the limited information gathered from 3.5 B- Chromosomes
other homopteran examples, an effort was made
to dene that the nature and kind of telomeric During the courses of systematic cytological
components that were found enhanced to estab- study in the case of Pseudococcus afnis chro-
lish as a C-banded heterochromatin. Moreover, mosomal complement that possesses supernu-
Panzera et al. (1992) and Prez et al. (1997) merary B chromosomes which were transmitted
based on their limited experience offer the opin- without the reduction during spermatogenetic
ion, especially of Triatoma meiotic systems, that courses that were found exhibiting a strong mei-
the tendency of the heterochromatin component otic drive, in such processes (Nur 1962a, b,
inferring to change in accordance with from one 1969). Prior to spermatogenesis, the B chromo-
chromosome to another or from proximal to dis- some was heterochromatic, but during prophase I
tal sites of the same chromosomes within a com- of spermatogenesis it became evident that even
plement. However, this characteristic cytological less condensed than the euchromatic set (i.e.,
feature was found on preferential localization of negatively heteropycnotic) and this change in
telomeric heterochromatic content of some condensation property apparently makes this sit-
instance cases alone probably thereby reecting uation possible for the Bs to segregate with the
upon C-banded components. These proposals are euchromatic set and be transmitted over to 90 %
in congruence with those of the Schweizer and of the offspring. Nur and Brett (1985, 1987,
Loidl (1987) hypothesis, but this type of chromo- 1988) have presented subjective data supporting
somal behavior is not in any way agreeable to that acquisition of the condensation property of
certain terms with other instance cases analyzed As and Bs during spermatogenesis seemed to
from other homopteran examples for the said infer that this situation is due to the presence of
purposes including the coccoid chromosome genotype that affects the rate of transmission of
systems. the Bs in males. However, it is somewhat clear
Ferraro et al. (1998) had undertaken an elobo- that this situation became evident because of the
rate proceedings in view of eliciting and appro- inuence of this genotype which has affected the
priating the preponderance of the ribosomal condensation property of B, but not the property
cistrons and upon highlighting of their cytologi- of heterochromatization. However, Klein and
cal localization based on the mealybug chromo- Eckhart (1976) theorized that difference between
somal preparations. This analysis had led to the Bs and regular chromosomes of Pseudococcus
results so obtained by means of the FISH tech- afnis could be due to changes occurring at the
nique and of subsequently staining the same with DNA sequences level. Another probable reason
silver nitrate solution for localizing NOR sighted was the differences observed between the
30 R. Sompalaym et al.

A and B sets that could be due to the occurrence licate or having replicated once, the euchromatic
of DNA of the two types of heterochromatin that sets replicated several times (Lorick 1970; Nur
being methylated. Thus, the percentage of 1966c, 1970, 1972).
5-methylcytosine in the DNA of P. afnis was The sex-specic association of the microor-
found to be higher in males than in females, and ganisms has led to the suggestion that they may
higher in females without Bs than in females with have a role in sex determination (Buchner 1965).
Bs (Scarbrough et al. 1984). However, the precise nature and role of endo-
symbionts in normal development has not been
clearly assessed. Biochemical and morphological
3.6 Polyploidy analyses of isolated endosymbionts have estab-
and Endosymbionts lished their prokaryotic characteristics (Houk and
Grifths 1980; Ishikawa 1989). The 16 s rRNA
In most species of mealybugs the polar bodies re- gene sequences of several homopteran insect
enter the egg and contribute to or give rise to endosymbionts including those of certain species
large polyploid cells (mycetocytes) that house of mealybugs and aphids, have been considered
intracellular bacterial symbionts (Brown 1965). for their role in the prevalence of phylogenetic
In some mealybugs, cells formed by polar bodies relationships among those species probed for
1 and 2 are known to be totipotent. In male those purposes (Munson et al. 1991, 1992;
mealybugs and in other coccoid families, one Kantheti 1994). However, the nature and extent
portion of the genome becomes heterochromatic of type of expression of the concerned gene
and the other becomes euchromatic (genetically inquisition during the course of insect develop-
active) in several tissues or organs (Tremblay ment are not clearly explained. Buchner (1965)
and Caltagirone 1973). These include the midgut, reported that extracellular symbionts are present
the Malpighian tubules, the salivary glands, in the females of Stictococcus but absent in the
oenocytes, and serosa (Nur 1967, 1972). One males. Most coccoids contain intracellular bacte-
characteristic of most of these tissues is that their ria or yeastlike symbionts present in the cyto-
nuclei later become polyploid as a result of endo- plasm of special cells, the mycetocytes (Tremblay
reduplication or endomitosis (Plate 3.6 Fig. 3, 5, 1977, 1989). The origin of the mycetocytes is of
9). During oogenesis, polar bodies do not degen- interest because it may vary between, as well as
erate; instead they re-enter the egg cell, and fuse within, families. Therefore, it appears probable
with each other and also with some of the cleav- that the origin of mycetocytes may have an
age nuclei and form polyploid cells called myce- important bearing on the pseudococcid genetic
tocytes. These mycetocytes are invaded by system (Hughes-Schrader 1948).
certain maternally transmitted microorganisms Interestingly, Kantheti et al. (1996) reported
generally referred as symbionts. Mycetocytes an isolation of the 16S rRNA gene sequenced
harboring such symbionts form an organ called segment, designated as P7 from an embryonic
mycetomes whose function is not known (Brown cDNA library of Planococcus lilacinus, which
1965; Nur 1977). Such symbionts are transovari- was found to be an encouraging attempt and by
ally transmitted to the next generation and thus hybridizing to the genomic DNA of females to
show maternal inheritance (Buchner 1965). the assay, but not to that of males. Interestingly
Euchromatization, however, is apparently not an P7 showed no hybridization to nuclei of either
essential step in the development of these tissues, sex, raising the possibility that it was extrachro-
because these types of tissues involved may vary mosomal in origin. Using electron microscopic
between congeneric species. Moreover, the fre- images, especially of P7 clones but not of P3,
quency of cells in which euchromatization occurs annealing was found to the adult female abdomi-
sometimes varies between individuals. However, nal organ called mycetomes. Electron micros-
in those nuclei in which the paternal genome copy has disclosed the presence of symbionts
remained heterochromatic, it usually did not rep- within the mycetocytes. Sequence analysis
3 Cytogenetics 31

showed that P7 is a 16 s rRNA gene conrming These bizarre genetic systems are of immense
its prokaryotic origin. P7 expression is detectable help in our attempt to understand further upon the
in young embryos of both sexes but the absence occurrence of a variety of sex-determining mech-
of P7 in third instar and adult males suggests that anisms prevailing in scale insects in the light of
the designated gene containing isolated gene their inherent property of inverse meiosis effec-
sequences assay and hence, consideration of pro- tively driving them through the efforts of holoki-
visional endosymbionts are the subject and object netic chromosome mechanics. Most species of
of sex-specic elimination/acquisition type of coccoids are bisexuals with extreme sexual
operating processes. dimorphism but due to precariousness of male
populations at times, some of them have become
parthenogenetic. These complex genetic systems
3.7 Mechanism of Sex appear invigorating due to the involvement of
Determination both the bisexual as well as the parthenogenetic
mode of reproduction. Another noteworthy fea-
In many species, sex determination is associated ture is inicted on them due to the deliverance of
with the inheritance of a heteromorphic chromo- quadrinucleate spermatid formation in many
some pair in one sex. However, not all species mealybug (bisexual) chromosome systems. It is
have evolved from a common ancestor that pos- thus possible to surmise that the various types of
sessed such an heteromorphic sex chromosome meiosis that were confronted within the scale
set. Rather, XXXY sex determination appears insect examples could have arisen in a derivative
to have arisen independently many times in evo- form or in a succeeding form from that of primi-
lution from the XXXO type form. The XXXY tive homopteran (aphidcoccid line) examples
sex chromosomes of ies and mammals also including aphid chromosome systems (XXXO
arose independently, but, the underlying mecha- system). It is thus possible to note that during the
nisms of sex determination are quite different and derivation processes it became inevitable in view
difcult to predict except in molecular terms. of the penchant situation prevailing with those
Coccoids are a unique and very peculiar group participants driving in through to the equatorial
of insects in view of their possessing a highly orientation of meiotic bivalents at rst meiosis
variable mode of sex-determining mechanisms. and of the preponderance of prereduction at
This situation becomes evident through the chiasma.
course of studying complex meiotic processes
incurred in a few select examples analyzed thus
far. Thus, this situation has led to the creation of 3.8 XXXO System
some academic interest by some earlier cytolo-
gists to pursue further upon attempting under- Sex determination in primitive coccoids could
stand the intricacies of meiosis and mitosis. have taken its initiation based on the XX ()XO
Interestingly, White (1973, 1978) took special () type of sex-determination mechanism.
interest in accommodating this opportunistic sit- Consequent upon this exigency, oogenesis is of
uation prevailing in mealybugs (scale insects) conventional type progressing through inverse
summarily termed as aberrant genetic systems, meiotic pathways, whereas spermatogenesis is
and Nur (1980) proclaimed unusual chromo- highly modied in most coccoids, mealybugs in
some systems but recent views indict them particular. In view of this unique situation, vari-
either as the more diverse or asymmetric able modes of expression pathways become
genetic system. Serendipity, as applied to these imminent as represented among analyzed primi-
scale insects, which are characterized by posses- tive margarodid examples. Currently, cytological
sion of a peculiar genetic system, was not found records have become known from margarodid
in any other animal system of comparable nature. assemblage of species that include taxa belong-
32 R. Sompalaym et al.

ing to Margarodidae, Ortheziidae, and Putoidae. cies of Puto demonstrated conventional meiotic
The cytological descriptions of these primitive chromosomal features. These species follow a
groups of species characteristically reveal that typical heterogametic mode of sex-determination
the sex of progeny is predetermined prior to and mechanisms, in which the males usually possess
at spermatogenesis; spermatozoa with the one chromosome less than that of females; char-
X-chromosome produce females and spermato- acteristically the example includes Puto species,
zoa lacking it produce males (Nur 1980). In this 2n = 1413; Puto albicans, 2n = 2019; and
extent, Brown (1977) placed primary emphasis Callipappus rubigonosus, 2n = 1413 (Brown
upon the coccoid chromosome system imparting and Cleveland 1968; Hughes-Schrader 1944).
the implicit nature of acquiring adaptive special- There are other taxa in which spermatogenesis is
ization and the same was found reected in the highly modied as was shown in meiosis of
progression of meiotic processes which in turn Protortonia and Matsucoccus gallicola dening
enabled categorizing into three types: (1) multiple sex chromosome systems. Surprisingly,
Margarodid assemblage, (2) Lecanoid types, and the only other report in which no morphologi-
(3) Diaspidid systems (Plate 3.8). In some cally identiable sex chromosomes were shown
Margarodid examples studied, spermatogenesis is represented by an example showing cytologi-
resembles that of conventional oogenesis, as is cal features for the whole Ortheziidae family,
especially evident in the case of Puto. Some spe- comprising 2n = 16 in both sexes (Brown 1958).

Plate 3.8 Representatives of other families of scale insects

3 Cytogenetics 33

3.9 Lecanoid System (i.e., imprinting) of and the activity status (of het-
erochromatization), of which the earlier process
In the Lecanoid chromosome type of coccoids seems likely to be an effective one at the ancestral
that exhibit a peculiar situation among coccoid stock and this attribute might reect in bringing
chromosome systems is one in which one hap- about differential condensation activity of the con-
loid set of chromosomes acquires heteropycno- cerned chromosomes. At this juncture, Brown (1977)
sis during the developmental course and also in felt that this situation appeared premature to the-
the germline cells. Those cells destined to become orize about or make any generalization unless
males acquire this status probably from mid- substantial molecular data were made available.
blastula onwards and persist through to adult life.
In the females, both sets of chromosomes in the
cell remain in the euchromatic state throughout 3.9.1 Parthenogenesis (Unisexual
the developmental course (Schrader 1921, 1923b; Reproduction)
Schrader and Hughes-Schrader 1926). The basis
for such an extraordinary situation in the mealy- While further pursuing the nature of the evolu-
bug chromosome is in the procession of acquisi- tionary trend involved during the course of sexu-
tion of the mechanism of heteropycnosis in male ality of scale insects, Hughes-Schrader (1948)
embryos and this involvement facilitates func- asserted that the prevalence of the parthenoge-
tional inequalities with respect to males that may netic mode of reproduction could be due to con-
point towards proclaiming them as physiological cordance with a higher incidence of disparity in
haploids, even though they have a duplex set in their reproductive potential. Thus, Hughes-
their nuclei (Plate 3.6). Brown and his group Schrader (1948) was able to discriminate bisexu-
have ventured into delineating the processes and als from those parthenogenetic ones and further
involvement of genetic mechanics of genomic suggested the appraisal of three fundamental
inactivation and of cytogenetics of heterochro- types of parthenogenetic products in them. Since
matinization processes in the genome (examples then, there have been considerable amounts of
include Planococcus, Phenacoccus, coccoid cytogenetic information procured by
Maconellicoccus, etc. of the family Brown and his associates that also afrmed that
Pseudococcidae and Laccifer of Kerridae). It is this situation based on cytogenetic surveillance
of interest to learn more about and probe further which acquired an innovative stimulus and pros-
the processes of heteropycnosis of the paternal pects including overall frequency of both bisex-
composition of the Lecanoid chromosomes and ual and parthenogenetic life cycle analysis from
as such it becomes imperative to note that this set among the select taxa of Coccoidea (Schrader
passed through the male phase but expressivity 1923b, 1931; Brown and Bennett 1957; Brown
was conned only to genetic male zygotes. 1963, 1964, 1965, 1966; Nur 1963, 1967, 1969;
Brown and Nur (1964) demonstrated earlier Hartl and Brown 1970). Subsequently, White
through their hybridization experiments that in (1973), who placed greater emphasis upon the
hybrid male embryos the mechanisms of hetero- parthenogenetic mode of reproduction and fur-
chromatinization of the paternal set can occur in thermore, on the implication and validity of het-
the cytoplasm of the foreign cell and thus this erosis during the courses of haplo-diploidy to
mechanism is not neccessarily a species-specic diplo-diploidy, was a matter of great antiquity.
characteristic, because heterochromatinization This and other cumulative studies (White 1978)
progression processes occur after several divi- have moved towards arriving at a conceptualiza-
sions of cleavage, and the paternal set must tion relating to efciency of homozygosity that
somehow seemed to have been marked (or would more likely to have an effective impact
learned) which could have been done or did prior upon haplo-diploids rather than diplo-diploidy.
to the entry of sperm into the egg (Chandra and Brown (1977), Hughes-Schrader (1948), and Nur
Brown 1975). Of the two processes, the marking (1971) have drawn inclinations towards suggesting
34 R. Sompalaym et al.

that it was at the cost of fragility and precarious- mated to have actively participated about eight
ness of males and of their implicit nature of effec- times during the course of evolutionary history
tiveness upon population measures, thereby (Brown 1965; White 1973). It was also felt that
imposing greater inconvenience on the part of the frequency of males (through Arrhenotoky) in
life-cycle strategies. Consequently, this kind of such populations was determined by the fre-
adaptiveness could have been driven towards an quency of haplo-diploids that arose in such con-
alternative mode of reproduction. Thus, the par- siderations. It is thus characteristic of any group
thenogenetic modes could be initiated by means with haplo-diploidy becoming much more
of adapting and involving either of Arrhenotoky inclined towards responding to the oppressive
or Deuterotoky or Thelytoky. But it was at the impact of environmental factors that accrued in
greater behest of Nurs (1969, 1970) concerted which sex ratio potential was deemed to have
efforts that had enabled him in eliciting and cat- been highly variable and it was also found to dif-
egorizing parthenogenomes each exhibiting dis- fer from species to species and even to the extent
tinct types of expression pattern. Subsequently, of genetic strains or of population level extremes.
Nur (1980) was also instrumental in document-
ing a revised format for parthenogenetic modes
of expression based on the following strategies: 3.11 Sex-Ratio Potential
whether the unfertilized eggs develop into males
(Arrhenotoky); or females (Thelytoky) or both In a majority of animal systems studied for the
(Deuterotoky); whether the males are haploid or prevalence of genetic-based sex-determining
diploid; and whether rst meiotic products mechanisms the extent was revealed of separate
between bivalents and oogonia remain the same sexes that direct each whether to become male or
(Gonoid thelytoky) or different (agonoid female, whereas in some taxa, hermaphroditism
thelytoky). may serve the primary mode of reproduction.
Whether a homomorphic (XXXX) or hetero-
morphic (XXXO) mode of sex determination
3.10 Arrhenotoky prevails in them, the sex ratio proportion seems
to be maintained in a harmonious manner (in a
Arrhenotoky is also called as haplo-diploid or 1:1 ratio). In such cases, where conventional dip-
haploid parthenogenesis in which males arise loidy exists, fathers and mothers often obtain
from unfertilized eggs. Males of haplo-diploids equal tness potential through to their sons and
may be referred to as impaternate because they daughters and hence, no sexual conict. But in
have no fathers. From the classical genetic point the case of alternative genetic systems, it becomes
of view, haplo-diploid species may have been essential to involve Trivers and Hares hypothe-
involved in recombinational processes (and sis (1976) that advocates the probabilities pre-
hence, Mendelian in character) inasmuch as they vailing for reproductive success of sons and
behave much to the same extent as those of sex- daughters that can differ markedly from parents.
limited characteristics, but possess no To that extent, they made a proposal in which
Y-chromosome. This, in a way, projects as a sort males and females were drawn into evolutionary
of male heterogamety in genetic characteristics; forces over the aspects of sex-allocation theory
on the other hand, Thelytoky offers a non- that depends on the inclusion and involvement of
Mendelian material thereby propelling it as a a particular genetic system (e.g., haplo-diploidy
reproductive devise. Haplo-diploidy or paternal genome elimination). In such
(Arrhenotoky), on the other hand, is a method of instances, a different set of reproductive trends
sex determination as well as a reproductive sys- seemed to follow in compliance with any biased
tem that involves replacement of an original sex- genetic transmission event that ensues which in
determining mechanism by an entirely new one turn can offer scope for the eventuality of sexual
under extraordinary circumstances. Hence, it conict. With particular reference to mealybug
could have occurred rarely in nature and was esti- examples, it becomes imperative to address the
3 Cytogenetics 35

DusingFischer formula (1976) that insists upon lies in the female germline tissues, suggesting
tness consequences of male and female off- that paternally inherited genes may still have the
spring that can vary with respect to the direct ability to inuence the fate of paternal chromo-
inuence or under duress of genetic and/or envi- somes in the germline but not in soma.
ronmental factors, even though selection prefers Scale insects consequently exhibit consider-
operating in such a way as to bring each into an able variations in their expression patterns based
equilibrium state. These generalizations can evi- on genetic and sex-determining mechanisms, in
dently be tested upon certain cases wherein genes spite of exhibiting similarity in their life-style
in fathers are only transmitted through daughters, strategies (Gullan and Kosztarab 1997; Nur
with sons being of no reproductive potential to 1980; Ross et al. 2011). Due to compulsions of
males. On the other hand, females gain tness their adaptive specializations imposed upon the
benets through both sons and daughters thereby morphology of male and female coccoids, how-
on demand for a possible expression of conicts ever, they differ enormously in terms of certain
over sex ratio. Orienting primarily towards other anatomical features. As is well-known
genetic consequences, the conventional diplo- among scale insects, males are winged hence
diploidy (XXXX system), becomes appar- motile, but with fragile stature although they
ent, in which case they still attempt to maintain a have a short life span based on acquisition of no
rigid sex ratio in the form of 1:1 because mothers feeding habituation, which may eventually suc-
and fathers do not vary through to the contribu- cumb to shortage of male populations. In con-
tions of daughters and sons and hence no sexual trast, females are robust, ornamental, and
conict. However, in unusual situations pertain- sedentary in habituation but have a longer life
ing to scale insects either haplo-diploidy or pater- span and are engrossed with gluttonous feeding
nal genome elimination (PGE) are offered as habits that might propel them to do better in con-
interesting but in extremity for an eventuality (as trolling sex-ratio propensities (Bull 1983).
the case may be). Earlier, Hughes-Schrader (1948) predicted that
On the other side, scale insects exhibit a dif- even though scale insects are besieged with vari-
ferent array of genetic systems, including haplo- able life-cycle strategies leading towards variable
diploidy as well as PGE offering as extremities. modes of genetic schemes, impulsively adaptive
The case of the mealybug (example Planococcus specialization could have driven them to acquir-
citri), provides an ideal system to pursue and ing Thelytoky and hermaphroditism. In fact
probe the kind of involvement and promotion of imposition of such kind of dwellings could have
sexual conict that it exhibits. It has PGE wherein been forced to serve as a clever device to dis-
the male component is in possession of haploid pense with the shortage of males. However,
nuclei, is (either it heterochromatized or) elimi- Brown (1977) contends that in spite of the com-
nated from meiotic cell lineage, and it is present plexities of several chromosome systems within
in somatic cells but untranscribed (Nur 1980). In the scale insects genetic systems, he contem-
terms of genetic mechanisms, the role of genomic plates acquisition of adaptive specialization, in
imprinting may be crucial. Scale insects are turn expanding towards acquiring exponential
known to represent the case in point of genomic taxonomic diversications. However, Nur (1980)
imprinting and imprinting of a paternal chromo- asserts that the fragility of the males may serve as
somal set alone is affected and also acts as a a primary instrument in an easing-out progres-
marker system for sex-determination mecha- sion during the courses of acquisition of a par-
nisms. In the case of mealybug paternal chromo- ticular mode of life-style activities or by adapting
somes especially of Lecanoids it is essential to to a particular chromosome system in succession.
point out that they remain in a latent state during The results obtained based on P. citri, have driven
the course of cell lineages. However, they get James (1937, 1938) and Nelson-Rees (1960) to
transmitted at the cost of a selective advantage. address that in Lecanoids, it appears possible to
Intriguingly, in P. citri, the site of genomic ascribe that females might play an impressive
imprinting of the paternal set of chromosomes role in selection and maintenance of sex-ratio
36 R. Sompalaym et al.

variability by their so adapting towards changes females prior to mating (James 1938; Ross et al.
and at times realigning to overcome any shortage 2010a). An increased understanding of sex allo-
of males. Changes in the sex ratio result in rein- cation theory in mealybugs might therefore yield
forcement of certain changes in developmental insightful opportunities to probe further into the
phases in the females which probably would potential ramications that drive in eliciting evo-
make arrangements towards shifting in the pro- lutionary advantages operating in proceeding
portion of procuring the requisite number of eggs towards extraordinary modes of sex-
and further upon imposing and resetting the determination mechanisms. The results obtained
paternal component onto the gambit of hetero- by Ross et al. (2011) upon P. citri experimenta-
chromatinization drive and in addition in an tions seem to point out appropriate levels that
effort to furthering towards a certain proportion were maintainable based on the role of high tem-
of eggs to be obtained profusely or curtailment. perature, older age at matings, and the starvation
All these adjustments mean amending changes in level, all of which seem to impress during the
contemplation within the scope of remodeling course of the consideration of sex-allocation the-
themselves towards acquiring and procuring a ories. These results may have inuenced changes
sufcient number of males. of expression patterns of female-biased sex
Consideration of imparting environmental ratios. But, they also propose that the effect of
forces upon such forces is based on the popula- temperature seemed rather weak and upon the
tion structure of offspring in responding to tness inuences of food restriction could have strongly
potential which would otherwise be driven implicated in reduced longevity and a transaction
towards differential expression patterns based on of the unusual schedule of male and offspring
the part of engrossing of established conict production across a female reproductive
drawn between parents and offspring. It is known lifetime.
that natural selection operates on those ratios in
which propelling forces rest on whether the par-
ents or offspring are in driving mode (Shuker 3.12 Recent Innovation Made
et al. 2009). It is also suspected that the offspring in Mealybug Genomes
can manipulate the sex-ratio potential thereby
affecting the sex allocation pattern. 3.12.1 Some Molecular Features
Trivers and Willard (1973) have conceived of
a pertinent opinion that environmental factors Heitzs (1928, 1929) unleashing of the opera-
could present oppressive effects on parents with tional denition of the term heterochromatin in
the possibilities of parental interference in an terms of its role in cell-cycle progression has trig-
effort to adjust sex allocation efcacy in the sex- gered momentum in cell biology to roll on
ratio potential. Environmental conditions experi- towards its own toll. This situation came as a
enced by parents can have direct interference natural ingredient for Brown (1966) to elicit suc-
during the course of sex allocation decisions pos- cinctly the ubiquitous nature of heterochromati-
sibly in one of two ways: either directly inuenc- nization serving as a pillar to the cytogenetic
ing parental conditions, or indirectly maintaining conundrum. While nurturing functional strate-
environmental factors as a cue to offspring t- gies, he succumbed to subdivide heterochromatin
ness. In P. citri, several environmental factors into two types: constitutive heterochromatin
have been explored especially pertaining to (CH) and facultative heterochromatin (FH).
embryogeny and other biological features of As a constituent of chromosomal architecture,
female reproduction. These measures include the constitutive heterochromatin comprises consid-
role of population density (Varndell and Godfrey erable portions of the genome in higher eukary-
1996; Ross et al. 2010a, b), impact of tempera- otes that include specialized chromosomal
ture (James 1937; Nelson-Rees 1960), and age of domains that are endowed with repetitive DNA
3 Cytogenetics 37

sequence specicities (e.g., centromeres, telo- for the study of genomic imprinting, operating at
meres, and nucleolar organizer regions). CH at the level of a gene and/or at a single chromosome
the molecular level is marked by distinctive or a whole chromosome set, wherein inactivation
structural changes incurred at the level of DNA of (1) one of the two X chromosomes in female
sequences, and with active participation of con- mammals and (2) a male haploid set of mealybug
stituent histones, and consequently upon its chro- chromosomes in a complement, serve as a unique
matin remodeling. In addition, recruitment of example for the consideration of epigenetic
HP1 (heterochromatin protein 1) at times serves phenomena.
as an essential ingredient of heterochromatin There is good evidence that the control of
structure. The interactions and dimerization transcription involves active participation of var-
activities of HP1 with that of DNA sequences, ious proteins which bind specically to methyl-
RNA, and histone moieties using appropriate ated DNA, wring in histone modication
combinations bring about repressive chromo- complexes, and eventually in local chromatin
somal complexes. This situation is thought to be remodeling processes.
widespread in many eukaryotic genomes and in Considering these features, the differential
some instances, this appears to be a conserved chromatin formation during the course of chro-
genome component lending its role appropriately mosome inactivation processes in the case of
from yeast to mammals (Nokayama et al. 2001; mammalian females and in the case of the pater-
Nielsen et al. 2001). The CH could also be diag- nal chromosomal set in male mealybugs repre-
nosed by highly methylated DNA sequences, sents a very clear case and an outstanding genetic
and/or histone modications that are enriched manifestation offered in the studies pertaining to
with, for example, methylated lysines an effort to understand the modes and methodol-
(H3K9Me3) and yet in depleted form in the case ogies involved during such processes (FH
of both H3K4Me3 and acetylated H4 (acH4). formation).
As the name implies, facultative heterochro- This exceptional situation offers immense
matin comes into force or effectiveness upon academic help in eliciting more on these topics;
their need to undertake any exigency purposes Lakhotia (2004) made efforts to shortlist achieve-
(such as gene regulatory activities). FH is a ments dwelling upon ongoing excitements that
euchromatic component but upon developmental prevail in the arena of epigenetical phenomena
cues acquires a highly compacted chromatin contributing towards the current phase of knowl-
structure to transform itself into an heterochro- edge available regarding heterochromatinization
matic comportment. In its native state, FH is progression. Several recent reviews have been
devoid of repetitive DNA sequences. Facultative forwarded detailing the prospects of mechanisms
heterochromatin differs from constitutive hetero- and functioning of various epigenetical programs
chromatin with respect to DNA sequence rear- that incorporate during gene regulatory activities
rangements but not at the nucleosomal level. At (Surani 1991; Li 2002; Cairns 2007; Kouzarides
the nucleosomal level, FH has many molecular 2007; Skiniotis et al. 2007; Bell and Spector
features similar to CH. From the pointing of its 2011). Of particular signicant and recent prog-
impaction among higher organisms and in cyto- ress are achievements heralded in the case of epi-
genetic context, FH affects only one of two genetic regulatory activities during genomic
homologous loci or homologous chromosomes, imprinting programming of the mammalian
or homologous chromosomal set. X-chromosome (Sado et al. 2005). On the other
Genomic imprinting is dened as a parent-of- hand, the present review focuses on recent
origin specic expression of selected or affected achievements made in our current understanding
gene(s), and has generally been associated with of the role of DNA methylation, histone modi-
specic changes in DNA methylation proles cations, and some points upon the chromatin
and in histone modication processes. Even remodeling processes pertaining to genomic
though there are numerous examples available analysis (e.g., Planococcus citri /P. lilacinus)
38 R. Sompalaym et al.

essentially based on chromosome organization of DNA methylation patterns. Vertebrate exam-

have been targeted to serve as a model genetic ples, on the other hand, have been shown as dem-
system. onstrating having acquired in the range of higher
levels of 5mC activities and were evidently docu-
mented, especially from among several higher
3.12.2 On Biochemical Paradigm animal examples. However, Bird (2002) is of the
opinion that it was not possible to corroborate
The regulation of gene expression plays a pivotal this situation to the same level of methylation
role in expediting complex phenotypes and in processes prevailing by 5Me between the verte-
differential expression patterns of epigenetic brate level to that of an insect system. The avail-
mechanisms, in which the role of DNA methyla- able data indicate varying levels of methylation
tion has been considered as playing an essential processes that do not seem to point out any con-
role in depiction of variable modes of operation served function. For example, the role of CpG
elicited during the course of chromosomal methylation as an epigenetic mark responsible
mechanics. In order to understand better the for genomic imprinting has been clearly estab-
functioning of DNA methylation processes is to lished in some mammalian examples (Feil and
learn more about its modes and methods and that Khosla 1999). Evidently, the case of human inac-
reect upon an operative course during distribu- tive X-chromosome in the female somatic chro-
tion patterns in the genome of interest. Cytosine mosomal complement serves as an ideal one for
DNA methylation has been demonstrated in sev- such kind of enquiry.
eral eukaryotic organisms and has been demon- On the other hand, the role of DNA methyla-
strated to play inquisitive roles in various tion in insects is still in its infancy. Thus, this
developmental activities. Variable portions of the situation could reect upon their leading a high
genomes are being subjected to the operative part diversity of life-cycle strategies prevailing from
of methylation with the help of 5-mehtylCytosine among individual cases pursued in each instance
(5mC) along the lengths of DNA sequence moi- for said purposes. The familiar one is the case of
ety. DNA methylation has been cited in numer- Drosophila melanogaster, in which DNA meth-
ous physiological functions depending on the ylation seems to be representing in an elusive
kind of model organisms utilized for said purpose way, because overall mechanisms prevail upon
and upon redesigning particular experimental developmental phases and more non-CpG meth-
protocols. Presence of DNA methylation in and ylation processes controlled by the role of Dnmt2.
around promoter regions is generally been In contrast, the case of Mamestra brassicae, a
thought to be associated with gene silencing pro- cabbage moth, based on HPLC analysis demon-
cesses and the loss of such kind of methylation strates the higher level of DNA methylation,
processes is reported to be accompanied by vir- which appears considerably closer to the stan-
tual transcriptional activation. dard level cited with respect to certain vertebrate
Several ideal examples can be cited inciting examples. Methylation experiments including
activities based on a methyl-transferase enzyme restriction enzymes as a parameter showed that
conglomerate that operates during such instances CpG sites were more spread out in the genome,
that have been profusely documented in several dispensing more towards the outer C of the
vertebrate and plant examples. In animals, the 5-CCGG-3sequences. However, results based
spectrum of methylation levels and patterns is on transposons are intriguing because mobile ele-
projected to reect upon a broader range and also ments are harboring and/ or congregating at or
indicate a highly variable mode of expression. proximal to repetitive sequences that seem heav-
Excepting cases such as Caenorhabditis elegans ily methylated, as was shown effectively in some
and Drosophila melanogaster, most invertebrate vertebrate and plant examples. However, a very
examples are reported in specicities reected in interesting case was that of Myzus persicae, a
indicating possession of a low to moderate level peach-potato aphid, wherein the enzyme systems
3 Cytogenetics 39

have been amplied drastically due to spurious to control the whole of the inactivation program
developmental activities of insecticide (E4 & (Cattanach 1974; Lyon 1999; Brown et al. 1991).
FE4) resistance genes and thus, forcing upon Characteristically, the mammalian inactive
detoxifying esterases that have been spurred up X-chromosome shows a typical characteristic
due to spurt in DNA methylation processes (Hick organization as scored by micrococceal
et al. 1996; Field et al. 2004). Overt expression endonuclease treatment, because transcriptional
patterns of CpG methylation in these cases might factors do (or can) not bind to its condensed
have reected upon the amplication events of domains (Pfeifer and Riggs 1991). On the other
the concerned genes, the situation of such kind hand, chromosomes play a different role in view
may be considered reecting upon the mechanics of the situation that coccoid genomes have
of methylation processes associated with the offered as a readily packed and amenable mate-
copious presence of DNA transposons as was rial of chromosome research in any cytogenetic
found necessary in the cases of several verte- and/or biochemical exploration activities.
brates and in transgene experiments carried out One of the unique features while characteriz-
in plants (Feil and Khosla 1999; Field 2000). ing genomes is to introduce an enhancing mecha-
The historic ndings of Schrader (1921, nistic driving so as to yield differential
1923b) and Hughes-Schrader (1948) in which organization of homologous chromosomal sets
male chromosomes were found to be character- dwelling in one point of reference which allows
ized by the presence of a haploid chromosomal one to pursue gratuitously such as, for example,
set acquiring precocious condensation property to pursue more upon the mechanisms of sex-
and thus, becoming inactive ones (in Lecanoids) determination, genomic imprinting processes,
or put into an ordeal of genomic elimination (in and into inactivation progression (Hughes-
Diaspidids) during the course of embryogenesis. Schrader 1948; Chandra and Brown 1975;
Brown and Nelson-Rees (1961) described such Peterson and Sapienza 1993). For example, the
an event occurring by elaborating on chromo- mealybug genome is unique because it is in pos-
somal mechanics imposed upon heterochromatic session of unusual chromosomal characteristics,
components by means of undergoing a faculta- involving diffuse centromeric organization
tively heterochromatinization program. (holokinetic activity) that encompasses inverse
The condensation property of the paternal meiotic processes, leading to a signaling of an
chromosomal set of mealybug chromosomes is unorthodox mode of cell-cycle manipulation in
correlated in parallel with the expression for males (Hughes-Schrader and Ris 1941; Brown
maleness. In mealybugs and other coccoids, and Nur 1964; Nur 1990). Thus, some of these
radiation-induced chromosomal fragments are unusual genetic bounties could have driven
not lost during mitosis but persist as stable enti- Chandra and his collaborators in attempting and
ties in nuclei of both sexes, demonstrating that exploring further these genomic contents (e.g., P.
the centromere is diffuse and that freshly broken lilacinus or P. citri) at the DNA sequence level
chromosomal ends can still form telomeres or and of modied version of bases in the DNA
telomerelike structures and regulate associated sequence organization.
functions (Brown and Nelson-Rees 1961; Employing appropriate but standardized bio-
Chandra 1963a). When broken chromosomes chemical protocols (Jamaluddin et al. 1979;
were transmitted by fathers to their sons, each Achwal and Chandra 1982; Achwal et al. 1983,
chromosomal fragment underwent heterochro- 1984; Karnik 1983; Deobagkar et al. 1982, 1986)
matization progression suggesting the presence have enabled their fruitful extraction of total
of multiple centers of chromosome inactivation. nuclear DNA content based on an Indian
This situation contrasts with the condensation Planococcus genome. These assays were utilized
property exhibited in mammalian females, for the purposes of studying the primary nature of
wherein the inactive X-chromosome is identi- methylation status by means of HPLC and chro-
able with a single center of activity and is thought matography which enabled disclosing the pres-
40 R. Sompalaym et al.

ence of signicantly higher amounts of 5-methyl methylation processes and were found to occur
cytosines in some portions of the genome. This about 2.5 times more frequently than those show-
was veried by dinucleotide analysis in which ing female specic methylation sequences.
5-mC seemed over represented with respect to Bisulphite modied DNA samples revealed an
other sequences (viz., CpA, CpT, CpC). interspersion of CpG and non-CpG methylation
Unusually higher amounts of 6-mAdinosine among sex-specic methylated sequences. This
(6-mA), 7-mGuanosine (7-mG) were also study also pointed out that there were more non-
encountered (Deobagkar et al. 1982). Achwal CpG methylates and/or at least twice as many
et al. (1983) reported a new protocol to isolate sex-specic methylated sequences found in
and characterize antibodies raised specically to males than in females. They thus based on those
5-mC, 6-mA, and 7-mG, a situation rarely found sequences that there could be offering a closer
in higher eukaryotes at that time. With the use of association between sex-specic methylated
immunobiochemical approaches they were able sequences located in transcriptionally silent chro-
to evaluate the samples to the same level of con- matin zones and those assays resistant to DNase I
tention to that of higher eukaryotic samples (viz., zones.
Drosophila, Human, etc.). Scarbrough et al. (1984) studies were based
Devajyothi and Brahmachari (1989, 1992) on the differential levels of 5-mC in the males
present evidence of obtaining homogeneous and females of Pseudococcus calceolariae and P.
extraction of DNA-methyl transferase enzyme obscurus and thus they were able to relate their
that were found specic to the test material ndings and that these results driving them to
(Planococcus citri/ P.lilacinus). The enzyme arrive at conclusions that males display higher
extracts exhibited a proactive mode of action and incidences of methylated sequences than those of
found preference for salt extraction techniques, female samples. Kantheti (1994) describes, with
because that appeared equivalent to routine the help of specic antibodies raised against
extraction protocols utilized in the case of mam- 5-mC, that there were more 5-mC localization
malian methylase assays. These results demon- spots identiable on male cells than on female
strate that the enzyme assays have had high ones in the case of P. lilacinus. There were also
specicities for denatured DNA substrates. two more studies reported on Planococcus citri
Mohan et al. (2002) using random stretches of P. (Bongiorni et al. 1999; and Buglia et al. 1999)
lilacinus DNA sequences, the technique of which whose genomic exploration of P. citri samples
was found to be helpful in delineating repetitive related to the prevalence of sex-specic cytosine
sequence analyses that were inferred as higher specicities but arrived at conicting inferences.
than those of other conventional sequences and Khosla et al. (1996) present evidence suggest-
were also found much higher than those of ing existence of specic DNA fragments that
Drosophila samples scrutinized and compared were perhaps offering to serve as a primary sig-
wherein GCs were found less frequent. Thus, nal during the elaborate mechanism as a contrib-
they infer based on this situation that seemed uting factor towards chromosomal imprinting
promising for the considerations upon inuenc- activities. Chromatin organization of Planococcus
ing on CpG dinucleotide sequence frequencies lilacinus was chosen for the purpose of extrapo-
which was found exclusively in those genomic lating rather than to consider offering as contrib-
samples. Methylation specic arbitararily primed utory factors to their functional spectrum.
(MS-AP), polymerase chain reaction (PCR), and Digestion of P. lilacinus samples with micrococ-
subtraction hybridization protocols were found cal nucleases showed 35 % of the male genome
helpful to Mohan and Chandra (2005) and thus to samples were different and the same were
describe the isolation and sequencing of sex- assayed and found to be more resistant to the
specic CpG methylation sequences that were introduction of enzymatic activities; as such
prevalent in genomic DNA samples of P. lilaci- these samples were designated nuclease resistant
nus. These sequences showed male specic chromatins (NRCs) fractions. This component
3 Cytogenetics 41

was present invariably in both sexes and through- towards processing of the heterochromatization
out the genome. However, cloned NRC DNA program. It was also felt that some nrc51 frac-
contained A + T rich sequences that were found tions were not accessible to MNases even in
revealing some homology towards that of sam- euchromatic chromosomes. For the same they
ples of mouse - satellites. Salt fractionation offer the suggestion that these sequences might
techniques revealed that these sequences were have been inferred to contribute towards
found to be matrix-associated. Based on these centromeric-type activity; instead, they were
experiments, they were tempted to offer some found to be dispensed with all along the length of
solutions in the form of those DNA sequences the chromosomes. It was well known that a sin-
present explicitly in NRC fractions and it was gle inactivation center exists in the case of the
possible to infer that this sample would serve as a mammalian inactive X-chromosome, in contrast
resource material for a future course of genetic to the situation prevailing in the mealybug chro-
studies. Thus, Khosla et al. (1996) ndings thus mosomes exhibiting multiple centers along the
are directed towards offering these parameters length of individual chromosomes that serve as a
that could as well be serving as a mode of strategy model system for the chromosomal inactivation
and further to consider them as putative centers program. In the light of these ndings, these are
for initiation of facultative heterochromatization the distribution specicities for nrc50 and nrc-
processes. However, they also cautioned that there 51fractions over the mealybug chromosome sam-
are other contributory factors that they might ples and considering them for their presence in
interact with this grand executive operation. In the the form of several heterogeneous NRCDNA
meanwhile a thorough scrutinization is necessary fragments and of enrichment within the unusu-
and required in an extensive way prior to arriving ally organized chromatins of the male would
at any kind of generalization in this regard. raise the possibility of examining them and per-
With the help of southern hybridization and haps serving as putative nuclear sequence loci in
FISH techniques, Khosla et al. (1999) provide the form of expression of multiple inactivation
results proclaiming the extrapolation of NRCs centers.
and further about prevalence of subdivisions of Extending these experiments as an extrapola-
these fractions in the form of two middle repeti- tion undertaken by Khosla et al. (1999), they pro-
tive sequences, designated as nrc50 and nrc51 vide descriptions based on their explicit pattern
samples. It was also found that they were differ- of expression of this unusual chromatin organiza-
entially organized within NRC composition and tion designated as NRC fractions during the
more interestingly they have enabled distinguish- course of cytologically identiable regions and
ing the sexes based on the placement of differen- during spermatogenesis and especially over
tial proximity. The NRCs were also found sperm nuclei even though their expression was
resistant to both MNase and DNAase I treatment on a maternal background. Furthermore, it was
and thereby enable exhibiting indistinct patterns made possible for them to infer that this compo-
that may help in identifying two sexes. Their nent can perpetuate through mitotic and meiotic
enrichment in NRC accounted to contain 50 and progression.
83 % for nrc50 and nrc51 type, respectively. It also appeared interesting that differential
Thus, 2530 % of samples remain resistant in chromatin organization forms procured from the
males but none in females. It has been shown samples of the mealybug (Planococcus lilacinus)
consistently that NRC is associated with the provide an important biochemical tool in consid-
nuclear matrix. On a nuclear matrix isolation eration of assessing and identifying maleness or
platform regarding male and female sample femaleness based on the presence or absence of
nuclei, it was found evident that the NRC frac- NRCs from the total genomic organization. Thus,
tions were present only in males but not in based on this important biochemical discovery, it
females. They further imply that it is the pater- was made possible for Khosla et al. (2006) to
nally derived hypomethylation set that drives hypothesize and suggest a biochemical model
42 R. Sompalaym et al.

that may be able to answer some of the vexing 3.12.3 Molecular Cytogenetics
problems confronted by geneticists included dur-
ing the course of understanding genomic imprint- HP-1 (Heterochromatin Protein-1) is a nonhis-
ing mechanics. They are of the opinion that by tone chromosomal protein with two highly con-
regulating NRC as a discriminating organization served domains. The amino terminal
in the paternal/maternal genome, it becomes pos- chromodomain (CD) has the capacity to bind
sible to discriminate male- oriented cells from either mono-, di-, or tri-methylated histone moi-
those of females while attempting to recognize ety (e.g., lysines) of H3 or H4 or others. The car-
facultatively heterochromatinized chromatin boxy terminal chromoshadow (CS) domains
organization in one or the other sex. At this junc- are involved in mediating protein protein inter-
ture, their inference was to ascribe that in the pre- actions (Eissenberg and Elgin 2000; Lachner
ceding zygote formation, the zygote is in et al. 2001). Historically, HP-1 was identied and
possession of the paternal genome in the form of isolated originally based on Drosophila melano-
the NRC positive state and as such, the status of gaster polytene chromosome heterochromatin
heterochromatin is in the form of negative effect. regions and subsequently, were procured from
Subsequent to sixth cleavage divisions, the said several other sources and from several other
NRC-positive paternal genome acquires hetero- organisms, considering these format posed us as
chromatization status based on the developmen- the basis for isolation and they were acquainted
tal decision made at some point in the ooplasm, through to the cloning experiments. By raising
in order to acquire a decision either to procure or antibody (CIA 9) against those subdivisions of
lose heterochromatin mediating proteins, thereby several homologues were procured. HP-1 are
acquiring a specic functional role based on a highly conserved and play a role in gene silenc-
NRC-positive or negative fraction. ing efforts in a diverse range of organisms (Singh
Subsequently, Mathur et al. (2010) present a and Georgatos, 2002). There appear to have been
genomic organization of another pseudococcid, instances wherein euchromatic zones require
Maconellicoccus hirsutus, thereby evaluating the HP-1 s for stabilization of their elongating tran-
obvious presence of the effective NRC fraction scripts (Vakoc et al. 2005).
and its mode of association with that of nuclear Epstein et al. (1992) were keen on extrapolat-
histone matrix content. They insist based on pre- ing the molecular biology of HP-1 and their ef-
vious experience that the afnity patterns ciency towards cloning and thus isolated several
between NRC and histone matrix form an impor- patterns of expression from Drosophila HP-1
tant binding property for a meaningful differen- homologues and the same were used to compare
tial expression especially eliciting developmental with samples drawn from several other sources
courses promoting the paternal mode of inheri- wherein their genomes were known towards
tance. The exhaustive study revealed by means of exhibiting heterochromatin programs in which
extraction and the identication of H3K27Me3, the role of HP-1 takes dominance. Because they
H4K20Me3, and H3K9Me3 proteins in both in knew that the degree of similarity between chro-
male- and in female-based samples and with a modomains (of polycomb) and HP-1 at the
signicant enrichment of H3K27M3 in the nucleic acid level it was found sufcient to detect
nuclear matrix of males compared to that of and isolate other genes from other organisms
females form an important and critical contribu- using low-stringency nucleic acid hybridization
tion. This particular biochemical component (Singh et al. 1991). Epstein et al. (1992) were
seems pointing towards and directing a cell-based exploring the possibilities of procuring HP-1
signal for a male sex-specic discriminating fac- homologues from several other sources; however,
tor. Furthermore, the analysis of cytologically they preferred to examine HP-1 s from mealybug
sorted nuclei indicates the presence of NRC in genomes because it was well-known that these
nuclei with different DNA content including the scale insect provide a robust example for such kind
haploid nuclei from males, is another interesting of consideration and thus may serve as a suit-
phenomenon disclosed in this genome. able target (Hughes-Schrader 1948; Nur 1990).
3 Cytogenetics 43

Thus, the coccoid genetic system is well recog- chromatin suppression. An extension of such
nized as one of the rst examples to pursue for kind of exploration made on the mealybug
examining parent-of-origin (parental imprinting) genome (P. citri) was represented and shown by
specic effects; subsequently, other examples intense staining of DAPI; but male cells were
were perused for said purposes including humans highlighted by discrete staining localization
(Solter 1998). But Epstein et al. (1992) were able rather than that of interphase nuclei. Only ecks
to describe their attempts by means of molecular of stainability marks were found over the euchro-
characterization of two chromodomain- matic portions, but the representation at the male
containing proteins called PCHET-1 and prometaphase stage was by and large very clear
PCHET-2 (for putative coccid heterochromatin (Cowell et al. 2002). Thus, they made an asser-
proteins 1 and 2), from the mealybug genome, tion towards this effect that the role played by the
Planococcus citri. They were able to prepare HP-1 protein in silencing of concerned genes is
cDNA encoding these proteins realized in clon- thought to be a conserved function (Nokayama
ing and in which it was shown that PCHET-1 et al. 2001; Nielsen et al. 2001).
seemed to have more potential than that of Recent studies on methylated histones have
PCHET-2. This fusion product was later utilized revealed that the level of methylation of the spe-
for exploring the expression patterns of cic lysines may have an important functional
PCHET-1 in other mealybug tissues and it was consequence for the assembly of heterochroma-
conrmed that it assisted in a male tissue-specic tin formation. Acetylation and methylation are
manner. However,, the specicities of tissue dis- the two types of post-transcriptional modica-
tribution of this protein may suggest the most tions known that have been identied in histones
sought after gene, but it was not at the level of (Wu et al. 1986). The histone code is a sugges-
correlating to the extent of identifying the male- tion made in which covalent modications may
specic heterochromatic chromosomal set. be brought about by the kind and mode of the
Moreover, PCHET-1 was not found traceable on participation of chromosomal proteins and as
female cells. Thus, they opine that PCHET-1 in such, a modication will have effects on driving
combination with other factors may help in pro- towards tissue-specic expression patterns.
viding a role for the sex-determination device. Kourmouli et al. (2004) have made observations
Many decades of concentrated work on het- that on the N-terminal tails of lysine 20 of H4, it
erochromatization in terms of cytological and is trimethylation of this lysine that occurs; but if
molecular characterization reveal that this chro- it is dimethylation of lysines it was shown to be
mosomal component (whether constitutive or associated with euchromatic portions of the
facultative) consists based on a macromolecular genomes (Fang et al. 2002; Kourmouli et al.
mould in the form of a repressive chromatin com- 2004). Furthermore, Kourmouli et al. (2004)
plex (Spofford 1976). It is well known that meth- have reported that in the murine examples, the
ylation of lysine 9 of H3 by Suv (3)9 methyl trimethylated lysine 20 of H4 (but not the Me(2)
transferase creates a binding site for HP-1 (CD) K20H4) establish specic relationships in the
resulting in the formation of a repressive protein presence of Suv(3)9 histone methyl transferase
complex; since it was considered the most robust activity, with that of Me(3)K9H3 thereby
histone modications known. accounting for epigenetic crosstalk between H3
While attempting to elicit mutual relation- and H4. Extension of such kind of study revealed
ships existing between heterochromatin, HP-1, that in the coccoid examples analyzed as a target
and trimethylated lysine 9 of H3 (Me(3)K9H3) as for action it was expounded that its expressivity
a requirement in analyzing X-chromosome inac- was observed on the facultative heterochroma-
tivation program is resolvable us in the mamma- tized paternal chromosomal set. They made a
lian examples including humans, Cowell et al. detailed assessment of this situation by means of
(2002) observed that there were elevated levels DAPI stainings where the heterochromatic
of trimethylation at the notied sites resulting in component forms a brightly stained property
44 R. Sompalaym et al.

(Epstein et al. 1992; Bongiorni et al. 2001; geted for such an exploration in order to delineate
Kourmouli et al. 2004). In the female mealybug chromosomal differences, especially pointing out
cells, Me(3)K20H4 is found scattered uniformly DNA sequences pertaining to differences occur-
throughout the chromosomal set. ring at the organizational level, to the extent of
Most imprinted loci may have key regulatory identifying methylated and nonmethylated
elements that are methylated on one of the paren- chromosomes.
tal chromosomes. For several of these differen- Bongiorni et al. (1999) have made a detailed
tially methylated regions, recent studies establish account of the structural organization in respect
that the unmethylated chromosome has a special- to both males and females, and the paternal
ized chromatin organization that is characterized derived haploid set was found to be
by nuclease hypersensitivity. In such a situation, hypomehtylated to that of the maternally derived
the question is raised as to whether associated chromosome. In males it is the paternally derived
chromatin features regulate the allele specicity hypomethylated haploid set that is heterochroma-
of DNA methylation at those imprinting control tized. To their surprise, in female embryos, half
regions. of the chromosomal complement was under-
Taking cognizance of a lead from the bio- methylated and thus, they inferred that the under-
chemical front that was well demonstrated from methylated chromosomal set in females
the reports of Scarbrough et al. (1984) and represented was of paternal origin, emphasizing
Devajyothi and Brahmachari (1992) and its rele- that DNA methylation could be at the basis of
vance to the possibility of establishing preva- imprinting phenomena at the chromosomal level.
lence of relationships between two states, DNA Thus they suggest that the two haploid sets are
methylation processes and chromosome imprint- imprinted by parental-of-origin-specic DNA
ing phenomena in the coccoid genetic system is a methylation with no correlation with the known
jerk in our understanding of chromosome gene silencing properties of the base
imprinting phenomena and is considered monu- modication.
mental in coccoid genetic research. In order to In their next venture (Bongiorni et al. 2001),
probe further this important component of scale they carried out experiments based on western
insects, Prantera and his team (2012) have initi- blotting and immunolocalization with uorescent
ated unearthing several molecular cytogenetic microscope-level observations upon mealybug
complexities. Following is a descriptive account genome P. citri. Their intuition was to identify a
of their research accomplishments. cross-reactive protein epilope whose properties
In order to probe and enlighten based upon suggest that of a homologue of Drosophila HP-1,
implications of molecular and chromosomal present in this species. By analyzing the distribu-
level investigations undertaken by Bongiorni tion patterns upon immunouorescence spottings
et al. (1999) who made a beginning towards they could infer the distribution of this HP-1-like
prevalence of procuring knowledge of the P. citri protein in male and female cells during the cell
genome of Italian origin. They utilized the RE/ cycle and in the early embryogenesis. It was evi-
NT technique (restriction enzyme directed in situ dent to point out this (HP-1-like) protein colocal-
nick translation) upon exploring of DNA izes with male-specic heterochromatin, thereby
sequence-level organization, thereby extrapolat- implying that this protein plays a role in the pro-
ing the P. citri chromosome (Ferraro et al. 2001). cess of facultative heterochromatization.
Concentrating specically based on MSPI and its However, they allay some doubts as to the
methyl-sensitive isoschizomer HPa II when used nature of the presence of P. citri HP-1-like pro-
as nicking agents, led them to make incisions into tein in embryos of both sexes which had led them
the genome by exposing organizational differ- to infer a protein factor was involved in the rec-
ences prevailing between homologous chromo- ognition of the imprint signal, suggesting that at
somes and subchromosomal regions (Prantera least there could be another factor provision
and Ferraro 1990). The P. citri genome was tar- which was found to be involved in the induction
3 Cytogenetics 45

of facultative heterochromatization and thus this exclusion of the heterochromatic chromosomes

factor should be male-limited in characteristics. from genetic continuum.
Moreover, as to the nature of C-banding staining, Earlier experience was driven to understand
it was not a strict cytological correlative measure that the HP-2 protein, a homologous HP-1 part-
to assign any heterochromatic role. It is well ner acquired from the D. melanogaster genome,
known that C-bands always coincide with consti- acts as a dominant suppressor of PEV, therefore
tutive heterochromatic composition. demonstrating a role involved in the structure
In their next exploration of coccoid chromo- and maintenance of heterochromatin structural
some systems, Bongiorni et al. (2004) concen- integrity. Implying the foregoing concept, Volpi
trated on detailing the inverted meiotic cycle et al. (2007) wanted to probe more of its effec-
established by means of indirect immune- tiveness upon the mealybug (P. citri) genome.
uorescent tapping. This issue drew special fea- With the help of an antibody raised against
tures because P. citri genetics revolves around Drosophila HP homologue epilope samples, they
diffuse centromeres and inverted meiosis. This acquired the set that was able to present cross-
study also focused specically on second meiotic reactive epilope and thus they designated the
division in which the male cell-cycle was mani- product as an Hp-2-like protein. Following the
cured by monopolar spindle activities and as a life-cycle patterns through to the male phase of
part of this special system, they dwelled more on the mealybugs revealed that they became with
the mode of meiotic drive enforced upon this acquainted with a heterochromatinized chromo-
genetic system. They were more interested and some set containing the requisite amount of anti-
engrossed on interpretation of meiotic spindle body deposition that was estimated by
activity in which the cytological preparations immunouorescent scanning. During the obser-
made were based on the use of an antibody that vations of the euchromatic chromosomes, HP-2-
was directed against insect tubulin. like impressions were sometimes traceable over
Earlier, Hughes-Schrader (1948) suggested the telomeric regions. The interplay between
the prevalence of monopolar spindle during male HP-2-like and HP-1 was critically examined
meiosis and interpreted that heterochromatic based on the introduction of ds RNAi experi-
chromosomes are the ones participating in such ments. Knocking out HP-1-like protein expres-
kind of activity. However, based on the introduc- sion with the introduction of the RNAi method
tion of recent protocols (Bongiorni et al. 2004) did not prevent the association of HP-2-like with
upon P. citri meiosis revealed that the spindle is facultative heterochromatization, thereby endorsing
associated with the euchromatic set facilitated by that the latter and its presence by binding to chro-
enhanced staining by DAPI that distinguishes matin is independent. They also utilized that this
each set by differential uorescent stainability. property extended to the processes of condensa-
The monopolar spindle could originate either tion or decondensation upon other cell types.
from a lack of centromeric duplication or from It is now certain that the HP-2-like protein
the lack of separation of duplicated centrosomes. binding to chromatin is a perquisite for faculta-
These authors were of the view that the formation tive heterochromatization assembly and it indeed
of a monopolar spindle and the lack of microtu- poses an interesting possibility that this compo-
bule binding by heterochromatic chromosomes nent must be tested by inactivation of HP-2-like.
are a necessary condition to ensure the noninde- Hp-2 antibody signals aggregate over distinct
pendent segregation of homologous chromo- chromatin areas, which identify the future chro-
somal sets at the second meiotic division. The mocenters after they have already been bound by
nonindependent assortment at the reductional HP-1-like. This suggests that the recruitment of
division together with the degeneration of the HP-2-like to the potential heterochromatic
heterochromatic spermatid nuclei formulate a domains depends on the presence of HP-1-like.
basis of the strong meiotic drive that leads to In adult tissues, where the heterochromatization
46 R. Sompalaym et al.

reversal occurs, the HP-2-like epitope is lost by lagging, abnormal condensation, segregation
the chromocenter remnants before the HP-1-like, defects), more so on structural maintenance com-
which thus seems to be insufcient to anchor ponents (SMCs).
HP-2-like to chromatin. It has also become evi-
dent that the strict colocalization of HP-2-like
with the chromocenter is not abolished in HP-1- 3.12.4 Chromatin Remodeling
like knockout embryos.
Molecular results based on some mammalian In many diverse organisms, gamete formation
examples, also including the mealybug genome, originates in a cytoplasmic, but highly conserved
were obtained independently by Kourmouli et al. structure, known as germ-line cysts. Germ-line
(2004) and Schotta et al. (2004) in an experiment cysts (or saclike structures) are composed of a
to certify the effect that Me(3)K9H3 employing group of cells; it is apparent that they took their
Me(3)K20H4 through the participation of HP-1 initiation from a single cell that underwent syn-
promoting heterochromatin formation appears to chronous cell divisions followed by incomplete
be a global-level event. But what was not clear cytokinesis. Modication of the chromatin struc-
about this was how HP-1 modulation is involved ture is one of the main epigenetic regulations con-
during gene activation processes in the case of ceived to carry out its operation in order to
the mealybug genome (P. citri; Bongiorni and undertake unique gene expression modalities. The
Prantera 2003; Bongiorni et al. 2007; Kourmouli male germ-line cyst is the organ that facilitates
et al. 2004). In contrast, acetylation of histone H4 executing the meiotic and/or post-meiotic mode
(AcH4) was found to be absent on the male- of gene regulation activity sharing during gameto-
specic heterochromatization processes (Ferraro genesis. The germ-line cyst morphogenesis
et al. 2001), whereas the depleted level of activa- acquires the responsibility of delivering the
tion of AcH4 was observed in the case of human respective genomic content to their destined sites.
X-chromosome inactivation (Jeppesen and Male meiosis of scale insects is interesting
Turner 1993). The foregoing issues have driven because meiotic sequence progressions proceed
to an understanding with a suggestion that Me(3) in accordance with those of inverse meiosis.
K9H3 via HP-1 to the Me(3)K20H4 pathway in Thus, during male meiosis each spermatogonial
an evolutionarily conserved mechanism of action precursor cell nucleus produces a bunch of syn-
for an epigenetic route to silencing large chromo- chronously dividing spermatogonia in a cytoplas-
somal domains by facultative heterochromatiza- mic cyst. Each spermatogonium divides four
tion (Chadwick and Willard 2004). times to produce a cyst of 16 primary spermato-
While establishing the prevalence of Me(3) cytes which then undergo two meiotic divisions.
K9H3 to HP-1to Me(3)K20H4 relationships in the Subsequently, each spermatogonium undergoes
case of P. citri genomes, Bongiorni et al. (2007) the rst equational and then the second reduction
proceeded further to interrelate the position of the division, which is characterized by specialized
HP-2-like protein (PCHET-2) based on RNAi movements directed and dictated by some
experiments. With the intermediation of ds RNAi unknown sources. But recent studies undertaken
(Fire et al. 1998) and by interference of knocking by Buglia and Ferraro (2004), Buglia et al.
down PCHET-2 in P. citri embryos, it was resolved (2009), and Bongiorni et al. (2009) have pro-
that the consequential depletion of the heterochro- vided some clues to learn more about the extent
matization pathway resulted in deheterochromati- and nature of expression, wherein these chromo-
zation with respect to gut cells and Malpighian somal movements were maintained and manipu-
tubules, whereas Hp-1 and Me(3)K20H4 in the lated by the monopolar spindle in which
same nuclei are either dispersed or absent. microtubules make physical connection with the
Embryos treated with ds RNAi (double-stranded euchromosomal set, rather than with the hetero-
RNA interference) targeting PCHET-2 also exhibit chromatic component as was contended earlier
chromosomal abnormalities (such as chromosome by Hughes-Schrader (1948). Even though Sciara
3 Cytogenetics 47

chromosomes practice monopolar spindle activi- H4K20Me3. This was found to be a consistent
ties, it seemed to be maintained through the expression pattern until the spermatid formation,
occurrence of monokinetic activity wherein mei- thereby demonstrating the supremacy of histone
otic products were manicured by sister-chromatid modications throughout the male part of the
cohesion (Esteban et al. 1997). meiosis. This situation is in congruence with that
By utilizing antibody-specic tracings, Buglia of Khosla et al. (1999, 2006) observations and of
and Ferraro (2004) describe an immunouores- their proposals advocating the presence of NRCs
cent staining protocol backed by enhanced active on paternal cell lineage until sperm maturation.
participation of fusomal elements, such as By now, it seems evident by pointing out that by
F-actin, included in the elaborate descriptions of the end of spermatogenesis PCHET-2 may be
factors that demarcate local morphogenesis losing its grip. Bongiorni et al. (2009) contend
essentially demarcating the cytoplasmic compo- that the presence and supremacy of H3K9Me2 &
sition of the male germ-line cysts. The co- 3 methylation processes dominate throughout the
localization of all these factors is an indication of course of gametogenesis, and with respect to the
the triggering action that could be measured by content of these proteins, they are in disagree-
densitometric proles which further enable in ment with the contention of Buglia and Ferraros
providing descriptions about the prevalence of (2004) observations. This pertains to the quan-
two kinds of sperms emerging but equipped with tum of differential distributions regarding
variable loads with respect to individual sperm euchromatic spermatids, because these products
content. take their origin from a single meiotic event.
A continuing search by Bongiorni et al. (2009) However, Buglia and Ferraro (2004) strongly
proceeded towards extrapolating procurement of dene that values they procured were essentially
the resources to be used during the gametoge- based on densitometric tracings, citing differing
netic processes and seemed to be in possession values with respect to H3K9Me2 & 3 and of
until early embryonic development. CIA9.
Immunolabeling of such components in order to In their subsequent study, Buglia et al. (2009)
probe has enabled identifying the presence of have elaborated mustering of resources pertain-
protein components such as H3K9Me2 & 3, ing to the development of female phases of
H4K20Me3, HP-2, and PCHET-2-like, that were gametogenesis of P. citri. Their results provide
concentrated in the paternal part of the meiotic the presence of a proteic component; this time the
stages throughout, but not in the female line to presence of HP1 and Su (var) 39 (a different
the extent of oocyte formation. On the other chromosomal protein), makes all the more impor-
hand, there were no traces of these modiers in tant contributions occurring during female gam-
the female gametogenesis. The redistribution of ete formation. Pertaining to the deposition of
epigenetic signaling marks in spermatids might variable contents of eggs it was found to contain
be related in the tracings of the processes con- two different kinds of cell inclusions, deposited
cerned with the establishment of parental imprint- in eggs, thereby categorizing in such a way as to
ing. Bongiorni et al. (2009) narrate the modes of act differently upon different ages of females.
operation through to the entry of sperm into the Based on these biochemical characteristics,
oocyte environment, where they are in posses- females with 40-days older age were considered
sion of distinct H3K9Me2 and 3 methylation as a younger group and those of 80-days old as an
marks that were found in the early pronucleus. older (aged) group. The ndings of larger
Observations were made of such kind of effect amounts of epigenetic factors accumulated in the
during the course of spermatogenesis indicating group of aged females in comparison to the
the presence in the form of heterochromatic com- younger ones was found to be an important
ponents decorated by H3K9Me2 & 3 and deciding factor. These studies have led to the
PCHET-2. Regarding the euchromatic compo- supposition of playing as a primary role based on
nent, it was shown containing HP-2-like and differential maternal contribution.
48 R. Sompalaym et al.

It was observed that the concept of genomic lated that the role of the mothers cytoplasmic
imprinting phenomena seemed to be lending environment might have been inicted by impo-
effective support in the cases of both Sciara and sition of environmental disturbances. Thus, dur-
coccoids, that the primary sex determination ing routine life-style courses, a one-to-one ratio
mechanism relied upon considering conse- in the case of sexually reproducing and one-to-
quences of occurrence of chromosome imprint- none in the case of parthenogenetic system, the
ing (Chandra and Brown 1975; Brown and sex ratio will operate in an expected line.
Chandra 1977). It also appears obvious in the However, if any change is incurred with respect
case of mealybugs, that possibly it was at the to the sex ratio it could possibly be envisioned
instance of mothers that enable directing and dis- and perceived as operating under constraints due
criminating the sex of her offspring. In addition, to the external forces that thrust upon maternal
the extension of this provision should yield environmental cues.
mechanistic support to the concept that mater- Currently, the mechanism of the genomic
nally controlled sex determination could also imprinting phenomenon is still unclear although
give way or leverage for control of the progeny the role of PCHET-2 and histone modications
sex ratio. Earlier, Nelson-Rees (1960) had con- seems evidently involved in effecting the faculta-
tended that the sex ratio in mealybugs uctuates tive heterochromatization process in the case of
among females and is markedly inuenced by the mealybug genome (P. citri). Females may
mothers age at conception towards the brood. In volunteer and might offer to alter the concentra-
both sexually reproducing and in parthenogenetic tion of those proteins in their eggs to their con-
mode of reproduction, the imprinting process ini- tention so as to modulate the sex ratio of their
tiates at and in the egg cytoplasm at the time of broods. Along this line, Buglia and Ferraro
the fertilization program. (2004) and Buglia et al. (2009) observations
Parental genomic inuences on the fate of off- point towards the situation that under the varied
spring development are evident in both inverte- concentration of CIA9-based positively stained
brate and vertebrates. Maternal effects are protein and of those of observations pertaining to
commonly mediated through deposition of the the eggs of females possessing variable amounts
cytoplasmic transcripts essaying protein products of proteins and at variable ages prior to mating
in oocytes during oogenesis in the female germ- should bring forth more differences in the egg
line. These then exert their effects on the fertil- chamber. They also apprise that females would
ized eggs and drive impulses upon early produce male-biased offspring whereas the oppo-
embryonic developmental processes (De Robertis site effect of maternal aging prior to mating was
et al. 2000; Gosden 2002), unlike some mamma- also observed in other studies.
lian examples that may provide guidelines for Prantera and Bongiorni (2012) postulated that
any kind of eventuality (Li et al. 2008). However, the embryonic cytoplasm at the blastoderm stage
there are no specic studies undertaken pertain- determines whether the paternal chromosomes,
ing to the operating mechanisms responsible for which are marked by DNA hypomethylation and
maintenance of genomic methylation imprints, H3K9me3 methylation marks, could be able to
even though the P. citri genome may serve as drive towards undergoing heterochromatization
very good material for such kind of expeditions. processes or not, and thereby giving rise to a
In view of this trepidation, it is possible to male or female embryo, respectively. Given the
infer that the mother can embark upon an initia- causative role and presence of PCHET-2 on
tion or directing a particular path towards the male-specic heterochromatin formation and
choice of her offspring and its bestowing effec- also based on the amount of PCHET-2 in the
tiveness on the sex-ratio potential. In promulgat- developing embryo, may prefer it as a crucial
ing the imprinting phenomenon, in terms of factor to drive the embryo either towards male-
evolutionary consequences with reference to a ness or femaleness. It is already envisioned that
choice-based progeny sex ratio, it was also postu- the effectiveness of facultative heterochromatini-
3 Cytogenetics 49

zation makes its presence in the seventh cleavage References

division onwards regarding male embryos and
moving in the form of a wave from one pole Achwal CW, Chandra HS (1982) A sensitive immuno-
chemical method for detection of 5mC in DNA frag-
towards the other, suggesting a graded distribu- ments. FEBS Lett 150:469472
tion on the part of PCHET-2. Inasmuch as Achwal CW, Iyer CA, Chandra HS (1983)
PCHET-2 could not possibly be observed either Immunochemical evidence for the presence of 5mC,
in sperm or in ooplasm, its presence only in the 6mC and 7mG in human, Drosophila and mealybug
DNA. FEBS Lett 158:353358
embryo should be at the courtesy of an early de Achwal CW, Ganguly P, Chandra HS (1984) Estimation
novo synthesis under the control of above-said of the amount of 5 methylcytosine in Drosophila
maternal factors. melanogaster by photoacoustic spectroscopy. EMBO
Investigations pertaining to nding answers to J 3(2):263266
Baer D (1965) Asynchronous replication of DNA in a het-
several questions have been raised and are still erochromatic set of chromosomes in Pseudococcus
pending for clarity with respect to our current obscurus. Genetics 52:275285
understanding of mealybug genomes and of their Bell JT, Spector TD (2011) A twin approach to unraveling
possibly related roles in expression patterns of epigenetic. Trends Genet 27(3):116125
Bird A (2002) DNA methylation patterns and epigenetic
chromosomal facultative heterochromatization memory. Genes Dev 16:621
(inactivation) processes. However, the molecular Bongiorni S, Prantera G (2003) Imprinted facultative het-
and cytogenetic data acquired by both the Indian erochromatization in mealybugs. Genetica
and the Italian investigators offer us highly com- 117:271279
Bongiorni S, Cintio O, Prantera G (1999) The relationship
mendable efforts since these contributions have between DNA methylation and chromosome imprint-
driven towards arriving at a mutual interest in the ing in the Coccid Planococcus citri. Genetics
form of a common platform of subjective 151:14711478
comprehension. Bongiorni S, Pasqualini B, Taranta M, Singh B, Prantera
G (2007) Epigenetic regulation of facultative hetero-
As part of a supposition made by Prantera and chromatinization in Planococcus citri via the Me(3)
Bongiorni (2012) and with those of the Khosla K9H3-HP1-Me(3)K20H4 pathway. J Cell Sci
et al. (2006) and Mathur et al. (2010) opinion that 120:10721080
NRC composition may have been inuenced by Bongiorni S, Mazzuoli M, Masci S, Prantera G (2001)
Facultative heterochromatization in parahaploid male
DNA hypomethylation and histone H3K9Me3 mealybugs: involvement of a heterochromatin-
methylation mark and furthermore, upon such a associated protein. Development 128:38093817
drive seemed to have made markings and then Bongiorni S, Fiorenzo P, Pippoletti D, Prantera G (2004)
spread over the whole of paternal but not mater- Inverted meiosis and meiotic drive in mealybugs.
Chromosoma 112:331341
nal chromosomes. Then, in the cleavage embryos, Bongiorni S, Pugnali M, Volpi S, Bizzaro D, Singh B,
some maternal factor(s) present in the ooplasm Prantera G (2009) Epigenetic marks for chromosome
might be able to regulate the imprinting process imprinting during spermatogenesis in coccoids.
by means of having acquired the requisite amount Chromosoma 118:501512
Brown SW (1958) The chromosomes of an Orthezia spe-
of PCHET-2 that gradually spreads from one cies (Coccoidea- Homoptera). Cytologia 23:429434
pole towards the other end of the developing Brown SW (1959) Lecanoid chromosome behavior in
embryo. A critical amount of regulated PCHET-2 three more families of the Coccoidea (Homoptera).
will then determine whether the paternal Chromosoma 10:278300
Brown SW (1961) Fracture and fusion of coccid chromo-
imprinted chromosomes will become heterochro- somes. Nature 191:14191420
matic, thus picking up the path leading towards Brown SW (1963) The Comstockiella system of chromo-
male embryonic development or will remain some behavior in the armored scale insects (Coccoidea:
euchromatic, thereby losing repressive histone Diaspididae). Chromosoma 14:360406
Brown SW (1964) Automatic frequency response in evo-
modications and NRCs, and that eventually by lution of male haploidy and other coccid chromosome
not acquiring the requisite amount of markers, systems. Genetics 49:797817
hence rely on the path leading towards female Brown SW (1965) Chromosomal survey of the armored
embryonic development. and palm scale insects (Coccoidea: Diaspididae and
Phoenicococcidae). Hilgardia 36:189294
50 R. Sompalaym et al.

Brown SW (1966) Heterochromatin. Science 151:417425 Chandra HS (1962) Inverse meiosis in triploid females of
Brown SW (1969) Developmental control of heterochro- the mealybug, Planococcus citri. Genetics
matization in coccoids. Genetics 61(No. 1, part 2, 47:14411454
Suppl):191198 Chandra HS (1963a) Cytogenetic studies following high
Brown SW (1977) Adaptive status and genetic regulation dosage paternal irradiation in the mealybug.
in major evolutionary changes of coccid chromosome Planococcus citri I. Cytology of X1 females and the
systems. Nucleus 20:145157 problem of lecanoid sex determination. Chromosoma
Brown SW, Bennett FD (1957) On sex determination in 14:310329
the Diaspine scale Pseudaulacaspis pentagona (Targ) Chandra HS (1963b) Cytogenetic studies following high
(Coccoidea). Genetics 42:510523 dosage paternal irradiation in the mealybug.
Brown SW, Chandra HS (1977) Chromosome imprinting Planococcus citri II. Cytology of X1 females and the
and the differential regulation of homologous chromo- problem of lecanoid sex determination. Chromosoma
somes. In: Goldstein L, Prescott DM (ed) Cell biology 14:330346
a comprehensive treatise, Academic press, New York, Chandra HS (1971) Inactivation of whole chromosomes
vol 1, pp 109189 in mammalian X-chromosomes. Nature 253:165168
Brown SW, Cleveland C (1968) Meiosis in the male of Chandra HS, Brown SW (1973) Regulation of
Puto albicans (Coccoidea-Homoptera). Chromosoma X-chromosome inactivation in mammals. Genetics
24:210232 78:342349
Brown SW, Nelson-Rees WA (1961) Radiation analysis Chandra HS, Brown SW (1975) Chromosome imprinting
of a lecanoid genetic system. Genetics 46:9831007 and the mammalian X chromosome. Nature
Brown SW, Nur U (1964) Heterochromatic chromosomes 253:165168
in Coccoids. Science 145:130136 Chauhan NS (1970) Genetic evidence of an unorthodox
Brown SW, Weigmann LI (1969) Cytogenetics of the chromosomal system in the lac insect, Kerria lacca
mealybug Planococcus citri (Risso). Chromosoma (Kerr). Genet Res 16:341344
28:255279 Chauhan NS (1977) Gene expression and transmission in
Brown CJ, Lafreniere RG, Powers VE, Sebastio G, Kerria lacca (Kerr). Heredity 38:155159
Balabio A, Pettigrew AL, Ledbetter DH, Levy E, Cook LG (2000) Extraordinary and extensive karyotypic
Craig IW, Willard HF (1991) Localization of the X variation: A 48-fold range in chromosome number in
inactivation centre on the human X chromosome in the gall-inducing scale insect Apiomorpha (Hemiptera:
Xq13. Nature 349:8284 Eriococcidae). Genome 43:255263
Buchner P (1965) Endosymbiosis of animals with plant Cowell IG, Aucott R, Mahadevaiah SK, Burgoyne PS,
microorganisms. Inter science, New York Huskisson N, Bongiorni S, Prantera G, Fanti L,
Buglia GL, Ferraro M (2004) Germline cyst development Pimpinelli S, Wu R, Gilbert DM, Shi W, Fundele R,
and imprinting in male mealybug Planococcus citri. Morrison H, Jeppesen P, Singh PB (2002)
Chromosoma 113(6):284294 Heterochromatin, HP1 and methylation at lysine 9 of
Buglia GL, Predazzi V, Ferraro M (1999) Cytosine meth- histone H3 in animals. Chromosoma 111:2236
ylation is not involved in the heterochromatization of DAiuto L, de las Heras JI, Ross A, Shen MH, Cooke H
the paternal genome of mealybug Planococcus citri. (2003) Generation of a telomere-based episomal vec-
Chromosom Res 6:13 tor. Biotechnol Prog 19:17751780
Buglia GL, Dionisi D, Ferraro M (2009) The amount of De Lange T (2005) The protein complex that shapes and
heterochromatic proteins in the egg is correlated with safeguards human telomeres. Genes Dev
sex-determination in Planococcus citri (Homoptera: 19:21002110
Coccoidea). Chromosoma 118(6):737746 De Robertis EM, Larrain J, Oelgeschlager M, Wessely O
Bull JJ (1983) The evolution of sex determining mecha- (2000) The establishment of Spemanns organizer and
nisms. Benjamin Cummings, Menlo Park patterning of vertebrate embryo. Nat Rev Genet
Cairns BR (2007) Chromatin remodeling! Insights and 1(3):171181
intrigue from single molecule studies. Nat Struct Mol Deobagkar DN, Muralidharan K, Devare SG, Kalghatgi K,
Biol 14(1):19891996 Chandra HS (1982) The mealybug chromosome system
Camacho JPM, Belda J, Cabrero J (1985) Meiotic behav- I: unusual methylated bases and dinucleotides in DNA
iour of the holocentric chromosomes of Nezara virid- of a Planococcus species. J Biosci 4:513526
ula (Insecta: Heteroptera) analyzed by C-banding and Deobagkar DN, Shankar V, Deobagkar DD (1986)
silver impregnation. Can J Genet Cytol 27:490497 Separation of 5-methylcytosine-rich DNA using
Carter W (1962) Insects in relation to plant diseases. immobilized antibody. Enzyme Microb Technol
Interscience Publishers/Willey, NewYork, 8:97100
pp 247265 Devajyothi C, Brahmachari V (1989) Modulation of DNA
Cattanach BM (1974) Position effect variegation in the methyl transferase during the life cycle of a
mouse. Genet Res 23:291306 Planococcus lilacinus. FEBS Lett 250:134138
Chadwick BP, Willard HF (2004) Multiple spatially dis- Devajyothi C, Brahmachari V (1992) Detection of CpA
tinct types of facultative heterochromatin of the human methylase in an insect system: characterisation and
inactive X-chromosome. PNAS 101:1745017455 substrate specicity. Mol Cell Biochem 110:103111
3 Cytogenetics 51

Dikshith TSS (1964) Chromosome behaviour in Laccifer Gavrilov IA, Trapeznikova IV (2010) Karyotypes of six
lacca (Kerr) Lacciferidae-Coccoidea. Cytologia previously unstudied European mealybugs
29:337345 (Homoptera: Pseudococcidae). Comp Cytogenet
Dikshith TSS (1966) Spermiogenesis in Laccifer lacca 4(2):203205
(Kerr) (Lacciferidae-Coccoidea). Cytologia Gosden RG (2002) Oogenesis as a foundation of embryo-
31:302308 genesis. Mol Cell Endocrinol 186:149153
Drozdovsky EM (1966) On chromosomal sets in some Greider CW (1995) Telomerase biochemistry and regula-
coccoids (Homoptera: Coccoidea). Entomologicheskoe tion. Cold Spring, NewYork, (CSH Laboratory Press),
Obozrenie 45(4):712714 [In Russian] pp 3568
Eissenberg JC, Elgin SC (2000) The HP-1 protein family: Gullan PJ, Kosztarab M (1997) Adaptations in scale
getting a grip on chromatin current opinion. Genet insects. Annu Rev Entomol 42:2350
Dev 10:204210 Hartl DL, Brown SW (1970) The origin of male haploid
Epstein H, James TC, Singh PB (1992) Cloning and genetic systems and their expected sex ratio. Theor
expression of Drosophila, HP-1 homologs from a Pop Biol 1:165190
mealybug, Planococcus citri. J Cell Sci 101:463474 Heitz E (1928) Das Heterochromatin der Moose I. Jahrb
Esteban MR, Campos MC, Perondini AL, Goday C Wiss Bot 69:762818
(1997) Role of microtubules and microtubule organiz- Heitz E (1929) Heterochromatin, chromocenter, chromo-
ing centers on meiotic chromosome elimination in mere. Ber Deutsch Bot Ges 47:274
Sciara ocellaris. J Cell Sci 110:721730 Heitz E (1933) Die Herkunft der chromocentren. Planta
Fang J, Feng Q, Ketel CS, Wang H, Cao R, Xia L, 18:571636
Erdjudumat-Bromage H, Tempst P, Simon JS, Zhong Hick CA, Field LM, Devousluire AL (1996) Changes in
Y (2002) Purication and functional heterochromatin the methylation of amplied Esterase DNA during loss
of SETs a nucleosomal histone & lysine 20- specic and reselection of insecticide resistance in Peach-
methyl transferase. Curr Biol 12:10861099 Potato aphids, Myzus Persicae. Insect Biochem Mol
Feil R, Khosla S (1999) Genomic imprinting in mammals: Biol 26:4147
interplay between chromatin and DNA methylation. Houk EJ, Grifths GW (1980) Intracellular symbionts of
Trends Genet 15:431435 the Homoptera. Annu Rev Entomol 25:161187
Ferraro M, Buglia GL, Romano F (2001) Involvement of Hughes-Schrader S (1935) The chromosome cycle of
histone H4 acetylation in the epigenetic inheritance of Phenacoccus (Coccidae). Biol Bull 69(3):62468
different activity states of maternally and paternally Hughes-Schrader S (1944) A primitive coccid chromo-
derived genomes in the Planococcus citri. Chromosoma some cycle in Puto sp. Biol Bull 87:167176
110(2):93101 Hughes-Schrader S (1948) Cytology of coccoids
Ferraro M, Epifani C, Bongiorni S, Nardone AM, Parodi- (Coccoidea: Homoptera). Adv Genet 2:127203
Delno S, Prantera G (1998) Cytogenetic character- Hughes-Schrader S, Ris H (1941) The diffuse spindle
ization of the genome of mealybug Planococcus citri attachment of coccoids, veried by the mitotic behav-
(Homoptera, Coccoidea). Caryologia 51(1):3749 ior of induced chromosome fragments. J Exp Zool
Field LM (2000) Methylation and expression of amplied 87:29456
esterase genes in the aphid Myzus persicae (S). Ishikawa H (1989) Biochemical and molecular aspects of
Biochem J 349:863868 endosymbionts in insects. Int Rev Cytol 116:145
Field LM, Lyko F, Mandrioli M, Prantera G (2004) DNA Jaipuriar SK, Teotia TPS, Lakhotia SC, Chauhan NS
methylation in insects. Insect Mol Biol (1985) A reinvestigation of the lecanoid chromosome
13(2):109115 system in Kerria lacca (Kerr). Cytobios 42:263270
Fire A, Xa S, Montgomery MK, Kostos SA, Driver SE, Jamaluddin M, Philip M, Chandra HS (1979) A rapid and
Nelin CC (1998) Potent and sporadic genetic interfer- gentle method for the salt extraction of Chromatin.
ence by double stranded RNA in C. elegans. Nature J Biosci 1:4959
391:306311 James TC (1937) Sex ratios and the status of the male in
Frydrychov R, Grossmann P, Trubac P, Vtkov M, Pseudococcinae (Hemiptera: Coccidae). Bul Entomol
Marec F (2004) Phylogenetic distribution of TTAGG Res 28:429461
telomeric repeats in insects. Genome 47(1):163178 James TC (1938) The effect of the humidity of the environ-
Gavrilov IA (2004) Taxonomic and cytogenetic studies of ment on sex ratios from over-aged ova of Pseudococcus
scale insects (Homoptera: Coccinea) of European citri (Risso) (Hemiptera: Coccidae). Proc R Entomol
Russia. Proc Zool Inst RAS 300:7782 Soc Lond: Ser A Gen Entomol 13:7379
Gavrilov IA (2007) A catalog of chromosome numbers Jeppesen P, Turner BM (1993) The inactive X-chromosome
and genetic systems of scale insects (Homoptera: in female mammals is distinguished by a lack of his-
Coccinea) of the world. Isr J Entomol 37:145 tons H4 acetylation, a cytogenetic marker for gene
Gavrilov IA, Trapeznikova IV (2007) Karyotypes and expression. Cell 74:281289
reproductive biology of some mealybugs (Insecta: Kantheti P (1994) Studies on a female-specic cDNA
Coccinea: Pseudococcidae). Comp Cytogenet clone and chromatin organization in a, Planococcus
1(2):139148 lilacinus. Ph.D thesis. IISc, Bangalore
52 R. Sompalaym et al.

Kantheti P, Jayarama KS, Chandra HS (1996) Mckenzie HL (1967) Mealybugs of California with tax-
Developmental analysis of a female-specic 16S onomy, biology and control of North American spe-
rRNA gene from Mycetome associated endosymbi- cies ( Homoptera: Coccoidea: Pseudococcidae).
onts of a mealybug, Planococcus lilacinus. Insect University of California Press, Berkeley/Los Angeles,
Biochem Mol Biol 26:9971009 p 525
Karnik PS (1983) Correlation between phosphorylated H Miller DR, Kosztarab M (1979) Recent advances in the
1 histone and condensed chromatin in Planococcus study of scale insects. Annu Rev Entomol 24:127
citri. FEBS 163(1):128130 Mohan KN, Chandra HS (2005) Isolation and analysis of
Khosla S, Kantheti P, Brahmachari V, Chandra HS (1996) sequences showing sex-specic cytosine methylation
A male-specic nuclease- resistant chromatin fraction in the Planococcus lilacinus. Mol Gen Genomics
in the Planococcus lilacinus. Chromosoma 274(6):557568
104(5):386392 Mohan KN, Ray P, Chandra HS (2002) Characterization
Khosla S, Augustus M, Brahmachari V (1999) Sex- of the Planococcus lilacinus, a model organism for
specic organization of middle repetitive DNA studying the whole chromosome imprinting and inac-
sequences in the mealybug Planococcus lilacinus. tivation. Genet Res 79(2):111118
Nucleic Acids Res 27(18):37453751 Mohan KN, SandhyaRani B, Kulashrestha PS, Kadandale
Khosla S, Mendiratta G, Brahmachari V (2006) Genomic JS (2011) Characterisation of TTAGG telomeric
imprinting in the mealybugs. Cytogenet Genome Res repeats, their interstitial occurrence and constitutively
113:4152 active telomerase in the Planococcus lilacinus
Klein AS, Echardt RA (1976) The DNAs of the A and B (Homoptera; Coccoidea). Chromosoma 120:165175
chromosomes of the Pseudococcus obscurus. Mohan KN, Jun G, Kadandale JS (2012) Mealybug as a
Chromosoma 57:333340 model for studying responses to high doses of ionizing
Kondo T, Gullan PJ, Williams DJ (2008) Coccidology. radiation. Curr Topics Ionizing Rad Res 6:101116
The study of scale insects (Hemiptera: Sternorrhyncha: Moharana S (1990) Cytotaxonomy of Coccoids
Coccoidea). Revista Corpoica Ciencia y Tecnologa (Coccidea: Homoptera). In: Sixth international sym-
Agropecuaria 9(2):5561 posium of scale insect studies, Part II, Cracow, Poland,
Kourmouli N, Jeppesen P, Mahadevhaiah S, Burgoyne P, August 612. Agricultural University Press, Cracow,
Wu R, Gilbert DM, Bongiorni S, Prantera G, Fanti L, pp 4754
Pimpinelli S, Shi W, Fundele R, Singh PB (2004) Munson MA, Baumann P, Clark MA, Baumann L, Moran
Heterochromatin and trimethylated lysine 20 of his- A, Vogtlin DJ, Campbell BC (1991) Evidence for the
tone H4 in animals. J Cell Sci 117:24912501 establishment of aphid eubacterial endosymbionts in
Kouzarides T (2007) Chromatin modications and their an ancestor of four aphid families. J Bacteriol
function. Cell 128(4):693705 173:63216324
Lachner M, OCaroll D, Rea S, Mechtler K, Jenuwein T Munson MA, Baumann P, Moran A (1992) Phylogenetic
(2001) Methylation of histone H3 lysine 9 creatsa relationships of the endosymbionts of mealybugs
binding site for HP-1, proteins. Nature 410:116120 (Homoptera: Pseudococcidae) based on the 16s rRNA
Lakhotia SC (2004) Epigenetics of heterochromatin. sequences. Mol. Phylogenetics and Evolution
J Biosci 29(3):219224 1:2630
Li E (2002) Chromatin modications and epigenetic Muramoto N (1980) A study of the C-banded chromo-
reprogramming in mammalian development. Nat Rev somes in some species of heteropteran insects. Proc
Genet 3:662673 Japan Acad Scien phys and BiolScien 56:126130
Li X, Ito M, Zhon F, Youngson N, Zuo X, Leder P, Nielsen SJ, Oulad-Abdelghani M, Oritz JA, Remboutsika
Ferguson Smith AC (2008) A maternal zygotic effect, E, Chambon P, Lesson R (2001) Heterochromatin for-
Zfp57, maintains both maternal and paternal imprints. mation in mammalian cells. Interactions between his-
Dev Cell 15:547557 tones and HP1 proteins. Mol. Cell 7:729731
Little BA (1957) General and applied entomology, 3rd Nelson-Rees WA (1960) A study of sex predetermination
edn. Edition Harper and Row Publishers, New York, in the mealybug Planococcus citri (Risso). J Exp Zool
pp 165173 144:111137
Lorick G (1970) Differential DNA synthesis in hetero- Nokayama J, Rice JC, Strahl BD, Allis CD, Grewal SI
chromatic and euchromatic chromosome sets of (2001) Role of histone H3 lysine 9 methylation in epi-
Planococcus citri. Chromosoma 31:1130 genetic control of heterochromatin assembly. Science
Lyon MF (1999) Imprinting and X-chromosome inactiva- 292:110113
tion. Results Prob Cell Different 25:7390 Nur U (1962a) A supernumerary chromosome with an
Mani MS (1989) Indian insects, 1st edn. Satish Book accumulation mechanism in the lecanoid genetic sys-
Enterprises, Agra, pp 103105 tem. Chromosoma 13:249271
Mathur V, Mendiratta G, Ganapathi M, Kennady PK, Nur U (1962b) Sperms, sperm bundles and fertilization in
Dwarkanath BS, Pande G, Brahmachari V (2010) An a mealybug, Pseudococcus obscurus Essig
analysis of histone modications in relation to sex- (Homoptera: Coccoidea). J Morphol 111:173199
specic chromatin organization in the mealybug Nur U (1963) Meiotic parthenogenesis and heterochroma-
Maconellicoccus hirsutus. Cytogenet Genome Res tization in a soft scale, Pulvinaria hydrangeae
129(4):323331 (Coccoidea: Homoptera). Chromosoma 14:123139
3 Cytogenetics 53

Nur U (1966a) Harmful supernumerary chromosomes in a Prez R, Panzera F, Page J, Suja JA, Rufas JS (1997)
mealybug population. Genetics 54:12251238 Meiotic behaviour of holocentric chromosomes:
Nur U (1966b) The effect of supernumerary chromo- Orientation and segregation of autosomes in Triatoma
somes on the development of mealybugs. Genetics infestans (Heteroptera). Chromosom Res 5:4756
54:12391249 Peterson K, Sapienza C (1993) Imprinting the genome:
Nur U (1966c) Non replication of heterochromatic chro- imprinted genes, imprinting genes and an hypothesis
mosomes in a mealybug Planococcus citri (Coccoidea- for their interaction. Annu Rev Genet 27:731
Homoptera). Chromosoma 19:439448 Pfeifer GP, Riggs AD (1991) Chromatin differences
Nur U (1967) Reversal of heterochromatization and the between active and inactive X chromosomes revealed
activity of paternal chromosome set in male mealy- by genomic foot printing of permeabilized cells using
bug. Genetics 56:375389 DNase I and ligation mediated PCR. Genes Dev
Nur U (1969) Harmful B-chromosome in a mealybug. 5:11021113
Chromosoma 28:280297 Prantera G, Bongiorni S (2012) chromosome cycle as a
Nur U (1970) Translocations between euchromatic and paradigm of epigenetics. Genetics Research
heterochromatic chromosomes and spermatocytes International ID : 867390:111
lacking a heterochromatic set in male mealybugs. Prantera G, Ferraro M (1990) Analysis of methylation and
Chromosoma 29:4261 distribution of CpG sequence in human active and
Nur U (1971) Parthenogenesis in Coccoids (Homoptera). inactive X-chromosome by in situ nick translation.
Am Zool 11:301308 Chromosoma 99:1823
Nur U (1972) Diploid arrhenotoky and automictic thely- Raju NG (1994) A study of the chromosomes in three spe-
toky in soft scale insects (Lecaniidae: Coccoidea: cies of Indian. Dissertation, Bangalore University,
Homoptera). Chromosoma 39:381401 Bangalore, Planococcus. M.Phil
Nur U (1977) Maternal inheritance of enzymes in the, Ris H (1942) A cytological and experimental analysis of
Pseudococcus obscurus (Homoptera). Genetics the meiotic behavior of the univalent X-chromosome
86:149160 in the bearberry aphid Tamalia (d'hyllaphis) Coweni
Nur U (1980) Evolution of unusual chromosome systems (Ckll.). J Exptl Zool 90:267326
in scale insects (Coccoidea: Homoptera). In: Blackman Ross L, Pen I, Shuker DM (2010a) Genomic conict in
RL, Hewitt GM, Ashburner M (eds) Insect cytogenet- scale insects: the causes and consequences of bizarre
ics. Royal Entomological Society, London, pp 97117, genetic systems. Biol Rev 85(4):807828
278 Ross L, Langenhof MBW, Pen I, Beukeboom LW, West
Nur U (1990) Heterochromatization and euchromatiza- SA, Shuker DM (2010b) Sex allocation in a species
tion of whole genome in scale insects (Coccoidea: with paternal genome elimination: clarifying the role
Homoptera). Development supplement:2934 of crowding and female age in the mealybug
Nur U, Brett BLH (1985) Genotypes suppressing meiotic Planococcus citri. Evol Ecol Res 12:89104
drive of a B-chromosome in the mealybug Planococcus Ross L, Dealy EJ, Beukeboom LW, Shuker DM (2011)
obscurus. Genetics 110:7392 Temperature, age of mating and starvation determine
Nur U, Brett BLH (1987) Control of meiotic drive of the role of maternal effects on sex allocation in the
B-chromosomes in the mealybug, Planococcus afnis. mealybug Planococcus citri. Behav Ecol Sociobiol
Genetics 115:499510 65:909919
Nur U, Brett BLH (1988) Genotypes affecting the con- Sado T, Hoki Y, Sasaki K (2005) Tsix silence xist through
densation and transmission of heterochromatic modication of chromatin structure. Dev Cell
B-chromosomes in the mealybug, Planococcus afnis. 9:159165
Chromosoma 96:201212 Scarbrough K, Hattman S, Nur U (1984) Relationship of
Nur U, Brown SW, Beardsley JW (1987) Evolution of DNA methylation level to the presence of heterochro-
chromosome number in mealybugs (Pseudococcidae: matin in mealybugs. Mol Cell Biol 4:599603
Homoptera). Genetica 74:5360 Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R,
Panzera F, Alvarez F, Sanchez-Rufas J, Prez R, Suja JA, Reuter G, Reinberg D, Jenuwein T (2004) A silencing
Scvortzoff E, Dujardin JP, Estramil E, Salvatella R pathway to induce H3-K9 and H4-K20 trimethylation
(1992) C-heterochromatin polymorphism in holocen- at constitutive heterochromatin. Genes Dev
tric chromosomes of Triatoma infestans (Hemiptera: 18:12511262
Reduviidae). Genome 35(6):10681074 Schrader F (1921) The chromosomes of Pseudococcus
Papeschi AG (1998) C-banding and DNA content in these nipae. Biol Bull 40:259270
species of Belastoma (Heteroptera) with large differ- Schrader F (1923a) The origin of the mycetocytes in
ences in chromosome size and number. Genetica Pseudococcus. Biol Bull 45(6):279302
76:4351 Schrader F (1923b) A study of the chromosomes in three
Parida BB, Moharana S (1982) Studies on the chromo- species of Pseudococcus. Archiv fr Zellforschung
some constitution in 42 species of scale insects 17:4562
(Coccoidea: Homoptera) from India. Chromosome Schrader F (1931) The chromosome cycle of Protortonia
Information Service 32:1820 primitiva (Coccidae) and considerationof the meiotic
54 R. Sompalaym et al.

division apparatus in the male. Z Wiss Zool Pseudococcidi (Homoptera: Coccoidea). Bollettino
138:386408 del Laboratorio di Entomologia Agraria Filippo
Schrader F, Hughes-Schrader S (1926) Haploidy in Icerya Silvestri. Portici 34:113135
purchasi. Z Wiss Zool 128:182200 Trivers RL, Hare H (1976) Haplo-diploidy and the evolu-
Schweizer D, Loidl J (1987) A model for heterochromatin tion of the social insect. Science 191:249263
dispersion and the evolution of C-band patterns. Trivers RL, Willard DE (1973) Natural selection of paren-
Chromos Today 9:6174 tal ability to vary sex ratio of offspring. Science
Shuker DM, Moynihan AM, Ross L (2009) Sexual con- 179:9092
ict, sex allocation and the genetic system. Biol Lett Tulsyan GP (1963) Studies on chromosome number and
5:682685 spermatogenesis in the lac insect Laccifera lacca
Singh PB, Georgatos SD (2002) HP1: facts, open ques- (Kerr). Curr Sci 32:374375
tions and speculation. J Struct Biol 140:1016 Vakoc CR, Mandst SA, Okachak BA, Blobel GA (2005)
Singh PB, Miller JR, Pearce J, Kothary R, Burton RD, Histone H3 lysine methylation and HP-1gamma are
Paro R, James TC, Gaunt SJ (1991) A sequence motif associated with transcription elongation through mam-
found in a Drosophila heterochromatin protein is con- malian chromate. Mol Cell 19:381391
served in animals and plants. Nucleic Acids Res Varndell NP, Godfray HCG (1996) Facultative adjustment
19:789794 of the sex-ratio in an insect (P. citri: Pseudococcidae)
Skiniotis G, Moazed D, Waitz T (2007) Acetylated his- with paternal genome loss. Evolution
tone tail peptides induce structural rearrangements in 50(5):21002105
the RJC chromatin remodeling complex. J. Biol Chem Venkatachalaiah G (1989) Characterization of heterochro-
282:2080420808 matin in chromosomes of Planococcus citri. XIII All
Solter D (1998) Imprinting. Intl J Dev Biol 42:951954 India Cell Biology Conference and Cell Biology
Spofford J (1976) In: Ashburmer & Novitski E (eds) Symposia. CCMB, Hyderabad
Position effect variation in Drosophila. Academic Venkatachalaiah G, Chowdaiah BN (1987) Air-drying
Press, London, pp 9551018 technique for the preparation of mosquito chromo-
Surani MAH (1991) Genomic imprinting: developmental somes. Nucleus 30(1, 2): 4446
signicance and molecular mechanism. Curr Opin Vitkova M, Karl J, Traut W, Zrzavy J, Marec F (2005) The
Genes Dev 1:241246 evolutionary origin of insect telomeric repeats
Tremblay E (1977) Advances in endosymbiotic studies in (TTAGG)n. Chromosomal Res 13:145156
Coccoidea. Va. Polytech. Ins. State University. Res Volpi S, Bongiorni S, Prantera G (2007) HP2-like protein:
Div Bull 127:2333 a new piece of the facultative heterochromatin puzzle.
Tremblay E (1989) Coccoidea endocytobiosis. In: Insect Chromosoma 116(3):249258
endocytobiosis: Morphology, physiology, genetics, White MJD (1973) Animal cytology and evolution, 3rd
evolution (eds.W. Schwemmler and G. Gassner). CRC edn. Cambridge University Press, Cambridge, p 961
Press, Boca Raton, Florida, pp 145173 White MJD (1978) Modes of speciation. W. H. Freeman,
Tremblay E, Caltagirone LE (1973) Fate of polar bodies San Francisco
in insects. Annu Rev Entomol 18:421444 Wu RS, Penuaz HT, Hatch CI, Bonner WM (1986)
Tremblay E, Tranfaglia A, Rotundo G, Iccarino FM Histones and their modications. CRC Crit Ren
(1977) Osservazioni comparate su alcune specie di Biochrem 20:201263
M. Mani

The insects coming under Hemiptera, Phenacoccinae, and Rhizoecinae (Downie and
Sternorrhyncha, Coccoidea, Pseudococcidae, Gullan 2005). This estimate was recently revised
and Putoidae are named as mealybugs (Williams in light of integrated molecular and morphologi-
2004). Following the application by Miller cal data, and only two subfamilies emerged:
(1975b), the family-group name Pseudococcidae Pseudococcinae and Phenacoccinae (Hardy et al.
(Cockerell 1905) was placed on the Ofcial List 2008). Molecular studies may either verify this
of Family-Group Names in Zoology (Melville grouping or show a different picture. By the study
1983) (type genus Pseudococcus Westwood of prokaryotic primary endosymbiont
1840). A (1968) attempted a higher classica- (P-endosymbiont) nucleotide sequences, Thao
tion of the Pseudococcidae based on a study of et al. (2002) showed that Antonina pretiosa
the characters of adult males of 17 species. The Ferris, presently included in the Sphaerococcinae,
scale insects are generally divided into two is closely related to the blue-green or blue-black
groups, namely the archeococcids and the neo- mealybugs of the genera Amonostherium
coccids. The archeococcids possess two to eight Morrison and Morrison, Australicoccus Williams,
pairs of abdominal spiracles, which are absent in Melanococcus Williams, and Nipaecoccus Sulc.
the neococcids (Koteja 2008). The family These genera are included in the Trabutininae, as
Pseudococcidae (mealybugs) belongs to the neo- discussed by Koteja (1974a, b).
coccid group. Pseudococcidae constitutes the second largest
After extensive studies on the labium of 84 family of Coccoidea, with more than 2000
species of Pseudococcidae, Koteja (1974a, b) described species and ca. 290 genera (Ben-Dov
proposed that the family is composed of four sub- 2006; Downie and Gullan 2004). Pseudococcids
families: Trabutininae, Rhizoecinae, occur in all zoogeographical regions of the world.
Sphaerococcinae, and Pseudococcinae. This Pseudococcids are distributed in different geo-
classication has gained wide acceptance. A graphical regions as follows: Australasian region
recent phylogenetic study, based on the analysis (459 spp.), Afrotropical region (298 spp.),
of nucleotide sequence data, supported the exis- Nearctic region (424 spp.), Neotropical region
tence of three subfamilies: Pseudococcinae, (283 spp.), Oriental region (431 spp.), and
Palearctic region (710 spp.). Of the described
species, pseudococcids are most abundant in the
M. Mani (*) Palearctic region and least numerous in the
Indian Institute of Horticultural Research, Neotropical area. There are about 2000 species of
Bangalore 560089, India mealybugs worldwide. In southern Asia, 353

Springer India 2016 55

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_4
56 M. Mani

species of mealybugs have been recorded under considerable taxonomic value. This is exempli-
61 genera of which 105 species occurred in India ed in certain species of Chorizococcus and
with maximum species reported from Karnataka Spilococcus. The distance between the base of
(40 species) followed by Tamil Nadu (35 spe- one antenna and that of the other is of consider-
cies). India is rich in species of Formicococcus able value in separating species, particularly in
Takahashi (10 spp.), Antonina Signoret (six spp.), certain members of Rhizoecus. Most coccidolo-
Dysmicoccus Ferris (12 spp.), and Paracoccus gists have placed little taxonomic emphasis on
Ezzat and Mc Connell (six spp.). The genera, the eyes of mealybugs. However, the presence or
which are endemic to the Indian region, are absence of eyes in Rhizoecus and related genera
Aemulantonina Williams, Coccidohystrix has proved to be taxonomically useful. The
Lindinger, Eriodes Green, Lankacoccus labium varies considerably in shape and form
Williams, Pedronia Green, and Pseudantonina and may be elongate and slender in some species,
Green (Williams 2004). while in others, it is short and broad; in certain
Identications of mealybugs in practically all species, there appear to be signicant differences
cases are based upon the adult female. A sum of in the shape of both the basal segment and the tip
the morphological characteristics of the mealy- of the rostrum. Some species exhibit a sclerotized
bug used in identication of species belonging to area on the derm just anterior to the clypeus. In
family Pseudococcidae are as follows: Anal ring some instances, this has been of taxonomic assis-
is always present, divided longitudinally into two tance. The body form normally elongate; legs are
halves, each with single inner and outer rows of normally present and usually well developed.
angular cells and three setae; in a few instances, Considerable taxonomic emphasis has been
the ring is very much reduced, the sclerotization placed on the mealybug legs in the past by certain
is slight, and the pores apparently are nearly or coccidologists. Denticle or tooth on the plantar
completely lacking. Two pairs of dorsal ostioles surface of the claw offers an especially excellent
are normally present in the adult female. In some key character for the recognition of this series of
species, the number of these structures may be genera. Although the denticle or tooth still gener-
reduced, or they may be entirely lacking; thus, in ally is quite helpful in dening the members of the
some forms, the posterior pair is clearly present, genus Phenacoccus, it cannot be completely relied
but the anterior pair is lacking; in a few forms, upon as exemplifying this group alone. In many
the ostioles seem to be lacking in the adult but are species of Chorizococcus and Spilococcus, this
present in the rst stage. Others lack ostioles in tiny denticle or tooth on the claw is present, and
all stages; nevertheless, the totality of their char- it occurs in combination with other characters
acters places them in this family. The antennae that are not at all typical of the Phenacoccus series.
have been used in diagnoses of mealybug genera The body is normally with lateral groups of
for a long time and even for species separation. pores and has enlarged, conical setae, which form
Hence, more emphasis has been placed on the cerarii, that at times are evident only on the anal
antennal structure than on any other physical lobes, occasionally lacking, normally with pores
detail. In Antonina and related genera and species of the trilocular type present, rarely lacking.
of Eumyrmococcus, antennae may be reduced to Tubular ducts of a distinctive type are normally
one or two segmented stubs. It has been noted present as cylindrical invaginations in the derm,
that in certain genera, exclusive of Rhizoecus, the tube usually more heavily sclerotized at its
Geococcus, and Pygmaeococcus, where the opening, and with one side of the inner end of
antennae are noticeably short, small, ve to six tube showing a delicate lamentous prolonga-
segmented, and geniculate, the comparative slen- tion. Combinations of these characters will dene
derness or stoutness of the normal cylindrical the few aberrant forms of mealybugs that are
antenna in relation to its length has proved of known to exist.
4 Taxonomy 57

Translucent dots or pores on the hind femur 1. Place the entire specimen in a 6-ml., 1-in.
and tibia have denite signicance for species handled porcelain casserole dish approxi-
segregation. In some mealybug forms, each hind mately half-lled with Essigs Aphid Fluid
coxa bears a cluster of pores at its base, and the (see formula below), cover with 1-inch
area in which these occur is usually wrinkled. watch glass, and heat (120130 F) to dis-
This pore cluster is taxonomically important for solve (1015 min). A lateral incision made
differentiating certain species. The trochanter between the mid- and forelegs will help to
usually possesses a long seta at inner distal end clear the specimens more rapidly.
and the variation in its length and thickness 2. Remove the porcelain dish from the hot plate
proved to be a useful distinguishing character in and tease out the body contents while the uid
species of the Allomyrmococcini. The stoutness is still hot.
or slenderness of the pseudococcid legs in rela- 3. Transfer the cleared specimen to a droplet of
tion to their length has proved to be of much gum-chloral hydrate or chloral-hydrate
taxonomic importance. medium (see formula below). Apply a cover
Clypeolabral shield structure seems to reach slip and heat the slide on hot plate until the
its greatest development in certain bamboo- medium boils slightly. The specimen is then
feeding species of the tribe Serrolecaniini, and conditioned for examination under the com-
sometimes reaches almost the same length as the pound microscope. (Polyvinyl alcohol is also
clypeolabral shield. The structure is now known considered a good temporary-type medium.
to occur in many species but sometimes it is The specimens should be transferred from
barely perceptible. The extension is present Essigs Aphid Fluid directly into the solution.)
mainly in grass-infesting species and occasion- Valuable specimens are recoverable from this
ally in mealybugs feeding on the other groups of medium for permanent embedding in Canada
monocotyledons but, apparently, never in balsam, although this should not be delayed
dicotyledon-infesting species. longer than 3 or 4 months.
Cerarii situated on the dorsum of the body,
their total number, the number of enlarged coni-
cal setae, the presence or absence of auxiliary
setae, and the presence or absence of the accom- 4.2 Permanent Mounts
panying sclerotization have proved to be impor-
tant specic taxonomic characters. The following steps are used in the preparation of
Ventrally, the anal lobe is often sclerotized, permanent pseudococcid mounts:
and the character of this pigmentation is some-
times used as a taxonomic feature at the generic 1. Place the entire specimen in a 6-ml., 1-in.
and specic levels. handled porcelain casserole dish approxi-
The presence or absence of a circulus is mately half-lled with Essigs Aphid Fluid
exceedingly helpful as a key character within a (see formula below), cover with 1-inch
genus. At times, they vary in size, form, or num- watch glass, and heat (120130 F.) on a hot
ber to such a degree as to be of taxonomic value. plate until the body contents are dissolved
In some genera, several circuli may be present. (30 min to 1 h). A lateral incision made
between mid- and forelegs will help to clear
specimens more rapidly.
4.1 Temporary Mounts 2. Remove the porcelain dish from the hot plate
and tease the body contents while the uid is
The following steps are used in the preparation of still hot. If the specimen is not thoroughly
temporary pseudococcid mounts: cleared, tease out the loosened body contents
58 M. Mani

and transfer the specimen to a fresh solution of 6. Transfer the specimens to cellosolve in a clean
Essigs Aphid Fluid. Add three or four drops of depression slide and leave in this solution for
the prepared staining solution, consisting of not less than 5, preferably 20, min.
either acid fuchsin, lignin pink, or erythrosine 7. Transfer the specimens to xylene in a clean
(stain No. 2) (see staining solution formulae depression slide and wash thoroughly for 1 or
below), or even more of this solution if a deeper 2 min.
staining is desired. Heat again until the speci- 8. Place the specimens in a droplet of Canada
mens have absorbed the stain (1530 min balsam on a glass-cover slide and apply the
depending on the specimens involved.) cover slip. Use as little balsam as possible to
3. Transfer the specimens directly into a clear facilitate examination under the compound
6-ml porcelain casserole dish half-lled with microscope, especially under the oil-
tetrahydrofuran (C4H8O) and tease out the immersion magnication.
remaining body contents and excess stain.
Leave the specimens in tetrahydrofuran for The formula used to prepare Essigs Aphid
not more than 5 min, since prolonged periods Fluid is as follows:
may cause shriveling. In the case of very frag-
ile specimens, add a few drops of tetrahydro- Lactic acid (reagent grade 85 %) 20 parts
furan to the Essigs Aphid Fluid before Phenol (saturated in distilled H2O) 2 parts
transferring straight to tetrahydrofuran; this Glacial acetic acid 4 parts
will prevent shriveling. Water (distilled) 1 part
4. Transfer directly into Canada balsam and
apply the cover slip. Specimens should be The formula used to prepare chloral-hydrate
transferred rapidly form tetrahydrofuran to medium is as follows:
balsam, as little carry-over of tetrahydrofuran
as possible. Air bubbles are often left under Gum arabic 1g
the cover glass because the solution evapo- Dextrose 1g
rates quickly, but they will ultimately work Chloral hydrate 10 g
their way to the edge of the cover glass. It is
advisable to burst these bubbles with a needle Iodine crystals 1/10 g
dipped in tetrahydrofuran solution before Glycerin 1 cc.
placing the mount on heat to cure. This curing Water (distilled) 1 cc.
should not be done at more than 100 F, and
30 min to 1 his required to sufciently harden The formulae used in preparing the staining
the mount. solutions Nos. 1 and 2 are as follows:
5. When the balsam has hardened, the cover slip
may be ringed with shellac or other suitable No. 1 Essigs Aphid 15 ml.
media to prevent later fracturing of the bal-
Acid fuchsin (2 % aqueous 20 drops
sam. It is good to remember that the clearing solution)
and straining process cannot be hurried. No. 2 Essigs Aphid 15 ml.
However, when the specimens are properly Fluid
cleared and stained and the mounting tech- Acid fuchsin (2 % aqueous 20 drops
niques are mastered, excellent mounts will solution)
result. Because of the high volatility of tetra- Lignin pink (2 % aqueous 20 drops
hydrofuran, some of the smaller and more
Erythrosin (2 % aqueous 20 drops
delicate mealybugs tend to collapse when
transferred into it. In such a case, step 3 should
be modied as follows:
4 Taxonomy 59

Staining solution No. 1 gives excellent results. the Australian mealybugs by Williams (1985),
One slight drawback, however, is that the speci- and the mealybugs of Central and South America
mens from certain lots may begin to fade after 3 by Williams et al. (1992). A systematic catalog of
or 4 months. Preliminary observations made over the mealybugs of the world (Insecta: Homoptera:
approximately a 2-year period indicate that the Coccoidea: Pseudococcidae and Putoidae) has
staining solution No. 2 tends to overcome this data on geographical distribution, host plants,
feature, at least to some degree. It is interesting to biology, and economic importance by Ben-Dov
note that the species vary in their response to (1994) and the mealybugs of Southern Asia by
staining, some turning to darker red than others Williams (2004). The above keys may be referred
after the same time in the staining solution. This for identication up to species level.
has been advantageous in certain instances, espe-
cially where two species are mixed on a single
host and are indistinguishable from each other 4.3 Field Identication of Major
when collected in the eld. In such instances, the Species of Mealybugs
specimens may be easily segregated by species
before they are mounted. All mealybug species resemble each other to the
Brief instructions for slide-mounting scales untrained eye, so it is very important that an
and mealybugs have also been provided by the expert is brought to identify the mealybug spe-
United States Department of Agriculture (USDA) cies involved. The following characteristics are
in their Systematic Entomology webpage. Keys useful for eld identication. The adult female
available in the identication of mealybugs are mealybug is considered for the identication of
the mealybugs of California by McKenzie (1967), body shape, size, and color (Table 4.1):

Table 4.1 List of mealybug species with eld-identifying characters with their respective images
Mealybug species Field characters Images of mealybug
Antonina graminis (Maskell) (Rhodesgrass mealybug)
Broadly oval to circular body; rotund in lateral view; dark
purple or brown body; without lateral wax laments;
enclosed in a white, felted sac that turns yellow with age;
usually with a long, slender, white waxy tube protruding
through a hole in the ovisac at the posterior end of the body.
Usually present on the crown or nodes of the grass host.
Ovoviviparous; rst instars are cream colored; legs absent.

Noxious bamboo mealybug (Antonina pretiosa)

Adult body, brown; about 23 mm in length; immature
stages (i.e., crawlers) yellow; generally found at the nodal
regions of various bamboos. Sooty mold occurring at the
nodal regions and long wax laments arising from the nodal
areas are common symptoms.

60 M. Mani

Table 4.1 (continued)

Mealybug species Field characters Images of mealybug
Coccidohystrix insolita (Green) (Brinjal mealybug)
Adult females are light yellowish green in color with many
long glassy laments; very little dorsal wax; secretes a
white, waxy ovisac up to six times as long as the body of the
female; immature stages with no secretion of thick layer of
mealy wax; the body being shiny yellow-green with
submedian gray spots on two abdominal and one thoracic

Dysmicoccus brevipes (Cockerell) (Pineapple pink

Body oval or rotund; pink or pink-orange; legs yellowish
brown; body covered by thin layer of white mealy wax
allowing body color to be visible, without bare areas on
dorsum; dorsal ovisac absent, a few lamentous strands on
venter; with 17 pairs of conspicuous lateral wax laments,
often slightly curved, posterior pairs longest, one third to
one half as long as body, anterior laments shorter than
posterior pairs. Occurring on all parts of plant, usually in
protected area. Ovoviviparous; eggs pink.

Dysmicoccus neobrevipes (Beardsley) (Pineapple gray

Body oval or rotund; gray or gray-orange; legs yellowish
brown; body covered by occulent white mealy wax,
without bare areas on dorsum; dorsal ovisac absent; a few
lamentous strands on venter; with 17 pairs of conspicuous
lateral wax laments, often slightly curved, posterior pairs
longest, one third to one half as long as body, anterior
laments shorter than posterior pairs. Primarily occurring on
the above-ground parts of the host. Ovoviviparous.

Dysmicoccus boninsis (Kuwana) (Gray sugarcane mealybug)

Body elongate or elongate oval; body gray; legs yellowish
brown; covered by white mealy wax, without bare areas on
dorsum; dorsal abdomen covered by lamentous ovisac;
with four to six short lateral laments, posterior pair longest
and thickest. Usually present in leaf sheaths of sugar cane or
other grass host. Oviparous; eggs yellow.

4 Taxonomy 61

Table 4.1 (continued)

Mealybug species Field characters Images of mealybug
Ferrisia gilli (Gills mealybug)
Body 25 mm in length and pinkish grey in color; often
covered with white wax secreted from a pore, creating the
appearance of two stripes (darker areas) on their backs.
Larger nymphs and mature females produce a network of
white laments (510 mm) that protrude from the back of
the insect.

Ferrisia virgata (Cockerell) (Striped mealybug)

Body elongate oval; body dark gray; legs dark brown;
covered by white mealy wax; with a pair of dark dorsal
stripes on the body measuring 45 mm in length with two
long tails; body covered with long slender crystal like
laments/glossy threads in all directions; without lateral
laments. Usually ovoviviparous; eggs hatch immediately
after laying.

Hypogeococcus pungens (Granara de Willink)

Body rotund to elliptical; rounded in lateral view; body pink
to pink-yellow; legs light yellow; dorsal ovisac present in all
instars, covering entire dorsum; very lamentous; mealy
wax lightly dusted over body; lateral laments absent.
Occurring on all above ground parts of plant, often in
clumps at nodes, usually in protected areas. Oviparous; eggs
pink, hatch soon after being laid.

Maconellicoccus hirsutus (Green) (Pink hibiscus mealybug)

Adult female elongate oval; 3 mm in length; body pink in
color sparsely covered with white waxy coating; no to few
lateral (side) wax laments; body fringe absent; no stripes
on the back; body uid dark red; anal laments short; ovisac
irregular and beneath the body; ovisacs covering orange eggs
while crawlers are orange to light brick red in color. Feeding
causes twisted or distorted foliage.

62 M. Mani

Table 4.1 (continued)

Mealybug species Field characters Images of mealybug
Nipaecoccus nipae (Maskell) (Coconut mealybug)
Body round; somewhat at dorsoventrally; body red to
brown-orange; covered by thick white or yellow-orange
wax, without bare areas on dorsum; dorsal ovisac absent;
with ten to 12 pairs of broad lateral wax laments, posterior
pairs longest and thinner; anterior pairs broad and conical,
longest lament about one fourth as long as body. Primarily
occurring on foliage of host. Apparently ovoviviparous;
dorsum with ve to eight waxy laments similar in shape
and size to those on lateral areas of thorax and head.
Specimens turn black in 70 % alcohol.

Nipaecoccus viridis (Newstead) (Lebbeck/Spherical

Body round or broadly oval; somewhat attened
dorsoventrally; purple; covered by thick white, creamy, or
pale yellow wax, without bare areas on dorsum; ovisac
covering dorsum; probably with ve or six pairs of lateral
wax laments. Primarily occurring on foliage and fruits of
the host. Apparently oviparous; eggs purple; dorsum
probably with waxy laments. Specimens turn black in 70 %

Acute mealybug (Oracella acuta)

Body red to pink; about 3 mm in length; without side
(lateral) wax laments. Generally found both underneath
bark and on needles of hosts.

Palmicultor browni
Body reddish brown to pink; about 3 mm in length; with
side (lateral) wax laments; no ovisac produced.

Palmicultor palmarum (Maskell) (Palm mealybug)

Body round or broadly oval; somewhat attened
dorsoventrally; body red-brown; some specimens covered by
thick occulent mealy wax, others with less dense wax,
without bare areas on dorsum; ovisac absent; with eight to
14 or 15 lateral wax laments, posterior laments longest
and broadest, sometimes coalescing, laments on anterior
thorax and head shorter and thinner, posterior pair about 1/8
length of the body. Primarily occurring on foliage of the

4 Taxonomy 63

Table 4.1 (continued)

Mealybug species Field characters Images of mealybug
Palmicultor lumpurensis
Body grayish pink, about 3 mm in length, with large
amounts of white wax visible on host plant; body with few
side (lateral) wax laments; no ovisac produced.

Paracoccus marginatus (Williams and Granara de Willink)

(Papaya mealybug)
Body light yellowish white; 23 mm in length, with many
lateral (side) wax laments; ovisacs present with greenish
yellow eggs; wax pattern on body lacking any stripes on its
upper surface (i.e., dorsum); ovisac position is beneath and
behind the body and can be as much as twice as long as the
body; female adults also possess a series of short waxy
caudal laments less than a quarter of the length of the body
around the margin. When preserved in 80 % alcohol, P.
marginatus turn black within 2448 h.

Phenacoccus madeirensis (Green) (Madeira mealybug)

Body oval; somewhat attened dorsoventrally; body gray;
legs red; covered by thin, white, mealy wax, with dark
dorsosubmedial bare spots on intersegmental areas of thorax
and abdomen; these areas forming one pair of dark
longitudinal lines on dorsum; ovisacs present with yellow
eggs; ovisac covering entire dorsum; with 18 pairs of lateral
wax laments, posterior pairs longest, about the same length
or less length of the body.

Phenacoccus solenopsis (Tinsley) (Solenopsis mealybug/

cotton mealybug)
Body oval, often quite large (5 mm); somewhat rounded in
lateral view; dark green almost black; legs red; covered by
thin, white, mealy wax, with dark dorsosubmedial bare spots
on intersegmental areas of thorax and abdomen; these areas
forming one pair of dark longitudinal lines on dorsum;
ovisac absent from dorsum, but well developed ventrally;
with 18 pairs of lateral wax laments, posterior pairs
longest, up to the same length of the body. Normally
occurring on the crown of the host; surface of lateral
laments rough.

64 M. Mani

Table 4.1 (continued)

Mealybug species Field characters Images of mealybug
Phencoccus solani (Ferris) (Solanum mealybug)
Body with short laments; absence of long tails; absence of
stripes on the body; fringe present; no ovisac; similar to Ph.
solenopsis, but in P. solani on the other hand, bare spots
absent; and it has a medial wax crest with faint submedial
bare areas on the abdomen forming a pair of extremely faint
longitudinal lines on dorsum.

Phenacoccus manihoti (Matile-Ferrero) (Cassava mealybug)

Female mealybugs are ovoid; 0.51.4 mm in length;
rose-pink and dusted with white, powdery wax; the eyes are
relatively prominent; legs are well developed and of equal
size; body segmentation is apparent; very short lateral and
caudal white wax laments in the form of swellings that
produce a toothed appearance to the body outline; body is
usually covered with a waxy, with tufts of occulent waxy
secretion at posterior end and around the margins. The
species always reproduces parthenogenetically.

Phenacoccus aceris (Apple mealybug)

Adult female 34 mm in length; with a sage green body
color visible through the white waxy coating; tails on the
caudal end of the mealybug are shorter than those of grape
mealybug; and the body color (green vs. pale purple)
distinguishes it from grape mealybug.

Phenacoccus herreni (Cox and Williams)

(Cassava mealybug)
Very close to Ph.manioti, but yellowish; reproduces

Phenacoccus peruvianus (Bougainvillea mealybug)

Adult females (about 3 mm in length); elongate oval;
grayish-white; lack marginal wax laments; produce
relatively long, white waxy ovisacs on the leaves and stems
of their host plants.

4 Taxonomy 65

Table 4.1 (continued)

Mealybug species Field characters Images of mealybug
Phenacoccus parvus (Morrison) (Morrisons small
Body oval to elongate, light yellow covered with thin white
wax powder with peripheral small wax laments of uniform
size (1718 mm); without bare areas; ovisac absent dorsally,
present ventrally, long and cylindrical, up to three times
length of body; with 18 pairs of lateral wax laments, all
about same length, about 1/8 or less length of body.
Occurring on roots and foliage of host.

Planococcus citri (Risso) (Citrus mealybug)

Body oval; slightly rounded in lateral view; body yellow
when newly molted, pink or orange-brown when fully
mature; legs brown-red; mealy wax covering body, not thick
enough to hide body color; with dorsomedial bare area on
dorsum forming central longitudinal stripe (more obvious
than on P. cus); ovisac ventral only, may be two times
longer than body when fully formed; with 18 pairs of lateral
wax laments, most relatively short, often slightly curved,
posterior pair slightly longer, laments anterior of posterior
pair small, posterior pair about 1/8 length of body.
Oviparous; eggs yellow.

Planococcus cus (Signoret) (Vine mealybug)

Body oval; slightly rounded in lateral view; body yellow
when newly molted, pink or orange-brown when fully
mature; legs brown-red; mealy wax covering body, not thick
enough to hide body color; with dorsomedial bare area on
dorsum forming central longitudinal stripe (not as obvious
as on P. citri); ovisac ventral only, may be two times longer
than the body when fully formed; with 18 lateral wax
laments, most relatively short, often slightly curved,
posterior pair slightly longer, laments anterior of posterior
pair small, posterior pair about 1/8 length of body.
Oviparous; eggs yellow.

66 M. Mani

Table 4.1 (continued)

Mealybug species Field characters Images of mealybug
Planococcus kraunhiae (Kuwana) (Japanese mealybug)
Body oval or rotund; slightly rounded in lateral view; dark
purple or red; mealy wax covering body, not thick enough to
hide purple body color; dorsomedial bare area either absent
or unobvious; ovisac not described in literature; 18 lateral
wax laments, most relatively short, straight, posterior pair
slightly longer, laments anterior of posterior pair small,
broader than on P. citri, posterior pair about 1/8 length of
body; surface of lateral laments rough.

Planococcus lilacinus (Cockerell) (Coffee mealybug/

Oriental mealybug)
Body rotund; conspicuously rounded in lateral view;
brownish red or tan; mealy wax covering body, in thick
segmental clumps on mature females; body color evident at
segmental lines; with dorsomedial bare area on dorsum
forming central longitudinal stripe or oval area; ovisac
absent; with 18 lateral wax laments, broad, convergent,
posterior pairs sometimes curved, others straight, all
laments about same length, about 1/8 length of body.
Primarily occurring on the fruit, stems, and foliage of host;
specimens have been reported on the roots of coffee.
Ovoviviparous; rst instars pale maroon; surface of lateral
laments rough.

Planococcus minor (Maskell) (Pl. pacicus Cox)

The mealybug undergoes four development stages for the
male and three for the female. The total developmental
period (egg to adult) lasts 2830 (28.79) days for the male
and 2830 (33.70) days for the female. The female lays
7132 eggs/mass for its entire life span. A male to female
ratio of 1:4.43 is recorded. Adult male lives shorter (14
days) than the female (411 days).

4 Taxonomy 67

Table 4.1 (continued)

Mealybug species Field characters Images of mealybug
Pseudococcus calceolariae (Maskell) (Citrophilus
Body oval; slightly rounded in lateral view; dark in color,
red when crushed; ostiole uid red; mealy wax covering
body, usually thick enough to hide body color except on
intersegmental lines; with longitudinal lines on dorsum
formed by bare areas occurring in submedial and
submarginal areas; ovisac ventral only; with 17 lateral wax
laments, most relatively short, straight except posterior
pair, which may be slightly curved, posterior pair longest,
about 1/4 length of the body. Primarily occurring on foliage,
stems, and fruit of host. Oviparous; eggs yellow or orange;
surface of lateral laments rough.

Pseudococcus jackbeardsleyi (Gimpel and Miller)

(Jack Beardsley mealybug)
Body light grayish in color and oval, slightly rounded in
lateral view; about 3 mm long with 17 lateral wax laments,
becoming progressively longer posteriorly of the body; anal
laments equivalent to body length or more; ovisac ventral
only covering hind part of the body; no stripes on the back;
body contents crushed are reddish brown; mealy wax
covering body, not too thick enough to hide the body color.

Pseudococcus longispinus (Targioni Tozzetti) (Long-tailed

Body oval, slightly rounded in lateral view; body color
variable from light yellow to gray, mealy wax covering body,
thin enough so that the body color shows through; with three
longitudinal lines on dorsum, with single, broad dorsomedial
line, with two thin submarginal lines; ovisac absent, with 17
lateral wax laments, with posterior pairs conspicuously
longer than others, posterior pair as long as or longer than

68 M. Mani

Table 4.1 (continued)

Mealybug species Field characters Images of mealybug
Pseudococcus maritimus (Ehrhorn) (Grape mealybug)
Body oval; slightly rounded in lateral view; body dark
orange or pink; body contents crushed dark orange; ostiole
secretion light orange; mealy wax covering thin enough so
that the body color shows through; sometimes with faint,
wide medial longitudinal line on dorsum; ovisac encloses all
but head of female; with 17 lateral wax laments, becoming
progressively longer posteriorly, anterior pair about 1/8
width of the body, straight, unusually thin, posterior pair
longest, varying from 1/4 to 1/2 length of body. Oviparous;
eggs orange.

Pseudococcus viburni (Signoret) (Obscure mealybug)

Body oval; slightly rounded in lateral view; pink or light
purple; mealy wax covering usually thin enough so that the
body color shows through; without longitudinal line on
dorsum; ovisac encloses all but head of female; with 17
lateral wax laments, becoming progressively longer
posteriorly, anterior pair about 1/8 width of body, straight,
unusually thin, posterior pair longest, varying from 1/4 to
1/2 length of body. Oviparous; eggs yellow.

Rastrococcus iceryoides (Green)

Body oval to round; slightly rounded to convex in lateral
view; light yellow; legs light yellow; mealy wax covering
thick, in median area forming medial longitudinal ridge on
thorax and abdomen; without longitudinal bare areas on
dorsum; ovisac ventral, copious, tilting posterior end of
female off of host substrate when fully developed, similar in
appearance to cottony cushion scale (Icerya purchasi
Maskell); lateral wax laments variable in number,
coalescing through time, when separate, broad at base
narrowing to rounded point at apex, ultimately forming
plate-like fringe around body, anterior laments nearly 1/2
as long as width of the body, posterior laments slightly
longer than others, about 1/4 length of body. Oviparous;
eggs honey yellow.

Rastrococcus invadens
Ovoviparous; a tuft of hairs in the anterior region; lateral
laments increase in length from anterior to posterior region;
infestation conned to midrib of the leaves.

4 Taxonomy 69

Table 4.1 (continued)

Mealybug species Field characters Images of mealybug
Rastrococcus mangiferae
Similar to R invadens, body without tuft of hairs in the
anterior region; lateral laments increase in length from
anterior to posterior region.

Rhizoecus and Ripersiella

Very small mealybugs (12 mm in length); body white to
yellowish white; lacking side (lateral) wax laments. Roots
infested with ground mealybugs generally have areas of
white wax present and these mealybugs may be visible with
use of a hand lens.

Saccharicoccus sacchari (Cockerell) (Pink sugarcane

Body elongate oval, often quite large (7 mm); convex in
lateral view; body pink; mealy wax thin, allowing body color
through; without longitudinal bare areas on dorsum; ovisac
ventral; lateral wax laments normally absent, one short pair
may be visible in the newly matured adult females.

Vryburgia amaryllidis (Bouche) (Lily bulb mealybug)

Body elongate oval, sometimes quite large (up to 4 mm);
slightly rounded in lateral view; body light to dark purple;
ostiole secretion clear or light yellow; legs pale; mealy wax
thin, allowing body color through; without longitudinal bare
areas on dorsum; ovisac large, covering body of female; with
two pairs of caudal wax laments, posterior pair longer and
broader than anterior pair, conical about three or four times
longer than the anterior pair, posterior pair about 1/8 length
of body. Occurring at bases of leaves of Haworthia and aloe
and similar hosts; also on the roots and bulbs of other
liliaceous host. Oviparous; eggs pink; surface of lateral
laments rough.

70 M. Mani

Table 4.1 (continued)

Mealybug species Field characters Images of mealybug
Vryburgia brevicruris (Short legged mealybug)
Small mealybugs (23 mm long); red to purple; lacking side
(lateral) wax laments; two thick wax laments arising from
tip of the abdomen.

Vryburgia trionymoides (DeLotto)

Color pinkish-purple; with a light coating of white wax over
the body; and thick white laments arising from the tip of
the abdomen. The pinkish-purple body color may be
obscured by the powdery wax coating.

Stemmatomerinx acircula
Body gray with white wax; about 23 mm long; some wax
seems to be lamentous; no lateral wax laments produced.

Trionymus haancheni (Barley mealybug)

Adult female is quite small reaching a length of
approximately 1/5 in. (5 mm); body in some cases covered
with a white waxy secretion that extends as thin wispy
laments along the edges of the body and at the posterior
end; body shape elongate-oval, segmented, rather slender,
and with well-developed legs.

The number of wax laments protruding from The second type is root mealybugs/soil mealy-
the side of the body. bugs/subterranean mealybugs living in the soil
Presence and length of wax laments at the and feeding on the roots.
end of the body (i.e., terminal wax laments).
Color of eggs (if present).
Presence of an ovisac (a waxy mass covering 4.4 Role of Taxonomy
the eggs). in Management
Stripes on the body. of Mealybugs
Color of uids when crushed.
Success in pest management tactics including the
There are two types of mealybugs. One is leaf biological control programs depends on the cor-
mealybugs/foliar mealybugs/arboreal mealybugs rect identication of both the biological control
infesting the plant parts above the ground level. agent and the pest species. In last few decades,
4 Taxonomy 71

there have been more than ve major outbreaks Acerophagus coccois Smith (Bento et al. 1999).
of mealybugs causing alarming damage to crops, The most trenchant point concerning the parthe-
as a result of accidental introduction. nogenetic species P. manihoti is that an outbreak
The pink cassava mealybug, Phenacoccus could occur in southern Asia with the accidental
manihoti Matile-Ferrero, appeared on cassava in introduction of just a single immature specimen.
Africa in 1973 and soon spread throughout the Following the introduction of the cassava mealy-
whole cassava belt. To locate the source of this bug into Africa, another introduced mealybug
mealybug and to compare it with a morphologi- appeared in West Africa in 19811982, causing
cally similar species, which causes almost identi- extensive damage to fruit trees including mango.
cal damage to cassava in northern Brazil and This mealybug was initially identied as an
Guyana, required a considerable amount of time. undescribed species already known from India
Specimens from Africa and northern South and Pakistan and was later described as
America on the microscope slides showed wide Rastrococcus invadens Williams (Williams 1986).
variation in characters, and the method adopted This species is usually scarce in some parts of
to ascertain any limits to this variation required India because it is controlled by the natural ene-
rearing cultures in the laboratory at different tem- mies (Narasimham and Chako 1988); the intro-
peratures. This method normally induces wide duction of the encyrtid Gyranusoidea tebyi Noyes
morphological variation in mealybugs, helping to from India to West Africa and its swift control of
determine the limits of environmentally induced the mealybug are hailed as another biological
variation (Cox 1982; Cox and Williams 1981). control success (Neuenschwander et al. 1994).
The knowledge that the species in Africa was Another mealybug species was introduced
pink-bodied and uniparental and the species from accidentally to the Caribbean area in 199394
northern Brazil and Guyana was yellow-bodied and has since then spread beyond, eventually
and biparental (later described as Phenacoccus reaching USA. This damaging species was rap-
herreni Cox and Williams) was obscured initially idly identied by taxonomists as Maconellicoccus
because the specimens used for this study were hirsutus (Green); its biological control was
dead and had been preserved in spirit, obscuring described in detail by Kairo et al. (2000), with
the body color. When the two species could be discussion of the costs and benets. M. hirsutus
identied satisfactorily on the microscope slides, is widely distributed throughout the southern
it became apparent that the pink cassava mealy- Asia, Africa, and other parts of the Old World
bug, P. manihoti, was present in Paraguay and including Australia, and is still causing damage
Bolivia (Williams et al. 1981); hence, a search for in some parts of India. The introduced natural
natural enemies could be implemented there. The enemies, mainly the parasitoids Anagyrus kamali
introduction of the parasitoid Apoanagyrus lopezi Moursi (already known in the Old World) and
(De Santis) from South America to Africa and the Gyranusoidea indica Shafee, Alam and Agarwal
success of the biological control program against (collected in Egypt), and the predator
P. manihoti were well documented by Cryptolaemus montrouzieri Mulsant, have
Neuenschwander and Herren (1988) and Herren brought the mealybug under control. In response
and Neuenschwander (1991). Thus, the taxo- to this outbreak, an identication manual for the
nomic information can be retrieved in case the area (Watson & Chandler 1999) and a taxonomic
mealybug introductions originate from this area. study of all the instars of M. hirsutus (Miller
Phenacoccus manihoti remains a threat to the 2002) were produced.
cassava areas of southern Asia, as does the yellow Yet another mealybug is causing concern in
cassava mealybug, P. herreni, which still causes the Caribbean area Paracoccus marginatus
problems in South America. Reduction of P. her- Williams and Granara de Willink, described from
reni populations is now under way, mainly Mexico and parts of Central America as recently
through the introduction of the parasitoids as 1992, has become a serious pest in the
Apoanagyrus diversicomis (Howard) and Caribbean islands, where it attacks numerous
72 M. Mani

Table 4.2 List of mealybug species, correct identity of which led to a successful biological control
Country of accidental Introduced parasitoid for classical biological
Mealybug species introduction control
Phenacoccus manihoti Matile-Ferrero Africa Apoanagyrus lopezi (De Santis)
Phenacoccus herreni Cox and South America Apoanagyrus diversicornis (Howard)
Rastrococcus invadens Williams West Africa Gyranusoidea tebyi Noyes
Maconellicoccus hirsutus Green USA Anagyrus kamali Moursi
Paracoccus marginatus Williams and Caribbean islands Acerophagus papayae Noyes and Schauff
Granara de Willink Pseudleptomastix mexicana Noyes and Schauff
Anagyrus loecki Noyes and Menezes
Paracoccus marginatus Williams and India Acerophagus papayae Noyes and Schauff
Granara de Willink Pseudleptomastix mexicana Noyes and Schauff
Anagyrus loecki Noyes and Menezes

plant species, especially papaya (Carica papaya). come under the existing keys, it may be named as
The mealybug has now reached the southern a new species.
USA. A search for natural enemies in Mexico
(Becker 2000) located three parasitoids that are Acknowledgement Dr. Sunil Joshi, Principal Scientist,
now in use in controlling the mealybug. An off- NBAIR, Bangalore is acknowledged for providing
shoot of the biological control program has been
a detailed study of all the instars of P. marginatus
by Miller et al. (2005). The mealybug had
affected Carica papaya and several other plants
in Guam, Sri Lanka, Palau, India; in all countries, A SA (1968) Morphology and taxonomy of the adult
the species was rapidly identied as P. margin- males of the families Pseudococcidae and Eriococcidae
atus by taxonomists facilitating quick introduc- (Homoptera: Coccoidea). Bull Brit Mus (Nat Hist)
Entomol Suppl 13:1210
tion of the parasitoids.
Arve S, Patel KG, Chavan S (2012) Phenacoccus sole-
Table 4.2 shows a list of mealybug species, nopsis: the white menace to global agriculture: popu-
which were introduced in some countries, and the lation dynamics, biology and chemical control of
parasitoid, whose correct identity led to a suc- mealybug, Phenacoccus solenopsis Tinsley on
Hibiscus rosa-sinensis. LAP LAMBERT Academic
cessful classical biological control.
Publishing, 156 p
The examples mentioned above show that the Beardsley JW (1965) Notes on the pineapple mealybug
new pest species that may have escaped detection complex with descriptions of two new species
at quarantine inspection of imported plant (Homoptera: Pseudococcidae). Proc Hawaii Entomol
Soc 19(1):56
material can be quickly recognized by the taxon-
Becker H (2000) Three alien wasps may curb scale pest.
omists and accurately identied. The taxonomists Agric Res 58:1617
can also suggest the correct area of the origin of Ben-Dov Y (1994) A systematic catalogue of the mealy-
the pest and report whether any existing speci- bugs of the world (Insecta: Homoptera: Coccoidea:
Pseudococcidae and Putoidae) with data on geograph-
mens in slide collections were parasitized, so that
ical distribution, host plants, biology and economic
the precise collection localities can be searched importance. Intercept Limited, Andover, 686 p
for natural enemies for use in classical biological Ben-Dov Y, Miller DR, Gibson GAP (2006) ScaleNet: a
control. This information requires access to database of the scale insects of the world. In: United
States Department of Agriculture (USDA). http://
important reference collections of insects and to
the relevant taxonomic literature. The above eld Borchsenius NS (1947) On the taxonomic signicance of
guides and taxonomic information are to be morphological characters of mealybugs (Coccoidea,
referred for the quick tentative identication up Pseudococcus). Akad Nauk Dok SSSR (Moscow) (In
Russian) 58:21092110
to the species level. If the specimen does not
4 Taxonomy 73

Bento JMS, de Moraes GJ, Bellotti AC, Castillo JA, Koteja J (1974b) On the phylogeny and classication of
Warumby JF, Lapointe SL (1999) Introduction of par- the scale insects (Homoptera, Coccinea) (discussion
asitoids for the control of the cassava mealybug based on morphology of the mouthparts). Acta Zool
Phenacoccus herreni (Hemiptera Pseudococcidae) in Cracov 19:267325
north-eastern Brazil. Bull Entomol Res 89:403410 Koteja J (2008) Xylococcidae and related groups
Borchsenius NS (1948) Notes on Pseudococcus com- (Hemiptera: Coccinea) from Baltic amber (In English;
stocki (Kuw.) and some allied species (Homoptera; Summary in Polish). Pr Muz Ziemi 49:1956
Coccidea), with descriptions of three new species. Mani M, Joshi S, Kalyansundaram M, Shivaraju C,
Bull Ent Res 39:417421 Krishnamoorthy A, Asokan R, Rebijith KB (2013)
Borchsenius NS (1949) Fauna of USSR Homoptera, A new invasive Jack Beardsleyi mealybug, Pseudococcus
Pseudococcidae. Akad Nauk Zool Inst 38(7):383 jackbeardsleyi (Hemiptera: Pseudococcidae) on papaya
Cockerell TDA (1905) Some Coccidae from the Philippine in India. Florida Entomol 96(1):242245
Islands. Proc Davenport Acad Sci 10:127136 McKenzie HL (1967) Mealybugs of California with tax-
Cox JM (1982) Revision of the New Zealand onomy, biology and control of North American spe-
Pseudococcidae (Homoptera: Coccidea) with an cies (Homoptera: Coccoidea: Pseudococcidae).
experimental study of morphological variation. Thesis University of California Press, Berkeley, 524 pp
submitted for the degree of Doctor of Philosophy of Melville RV (1983) Opinion 1247 Dactylopius Costa,
the University of London and for the Diploma of (Nov. 1829) and Pseudococcus Westwood, 1840
Membership of the Imperial College, London, 388 pp (Insecta Homoptera): designation of type species. Bull
Cox JM, Williams DJ (1981) An account of cassava Zool Nomencl 40:7780
mealybugs (Hemiptera: Pseudococcidae) with a Miller DR (1999) 2002. Identication of the Pink Hibiscus
description of a new species. Bull Entomol Res Mealybug Maconellicoccus hirsutus (Green)
71:247258 (Hemiptera: Stemorrhyncha: Pseudococcidae). Insecta
Downie DA, Gullan PJ (2004) Phylogenetic analysis of Mundi 13:189203
mealybugs (Hemiptera: Coccoidea: Pseudococcidae) Miller DR (1975) Dactylopius Costa, 1835 and Pseudococcus
based on DNA sequences from three nuclear genes, Westwood, 1840 (Insecta Homoptera): proposed desig-
and a review of the higher classication. Syst Entomol nation of type-species under the plenary powers with pro-
29:238259 posed suppression of Diaprosteci Costa, 1828. ZN. (S.)
Downie DA, Gullan PJ (2005) Phylogenetic congruence 2056. Bull Zool Nomencl 31:146153
of mealybug and their primary endosymbionts. J Evol Miller DR, Miller GL, Hodges GS, Davidson JA (2005)
Biol 18(2):315324 Introduced scale insects Hemiptera: Coccoidea) of the
Ezzat YM, McConnell HS (1956) The mealybug tribe United States and their impact on U.S. agriculture.
Planococcini (Pseudococcidae: Homoptera). Bulletin Proc Entomol Soc Wash 107(1):123158
A (Maryland Agricultural Experiment Station), Narasimham AU, Chako MJ (1988) Rastrococcus spp.
University of Maryland, Agricultural Experiment (Hemiptera: Pseudococcidae) and their natural ene-
Station, College Park, no. 84, 108 p mies in India as potential biocontrol agents for R.
Ferris GF (1950) Atlas of the scale insects of North invadens Williams. Bull Entomol Res 78:703708
America (series V). The pseudococcidae (Part I). NBAII (2011) Annual report, National Bureau of
Stanford University Press, Stanford, 278 p Agriculturally Important Insects (ICAR), Post Box
Gullan PJ, Martin JH (2003) Sternorrhyncha (jumping No. 2491, H.A. Farm Post, Bellary Road, Bangalore
plant-lice, whiteies, aphids and scale insects). In: (Karnataka, India), 136 p
Resh VH, Carde RT (eds) Enclyclopedia of insects. Neuenschwander P, Herren HR (1988) Biological control
Academic Press, Amsterdam, pp 10791089 of the cassava mealybug, Phenacoccus manihoti, by
Hardy NB, Gullan PJ, Hodgson CJ (2008) A subfamily- the exotic parasitoid Epidinocarsis lopezi in Africa.
level classication of mealybugs (Hemiptera: Philos Trans R Soc Lond B 318:319333
Pseudococcidae) based on integrated molecular and Neuenschwander P, Boavida C, Bokonon-Ganta GA,
morphological data. Syst Entomol 33(1):5171 Herren HR (1994) Establishment and spread of
Herren HR, Neuenschwander P (1991) Biological control Gyranusoidea tebygi Noyes and Anagyrus mangicola
of cassava pests in Africa. Annu Rev Entomol Noyes (Hymenoptera: Encyrtidae), two biological
36:257283 control agents released against the mango Mealybug
Keifer HH (1946) Isopropyl alcohol and phenol used in Rastrococcus invadens (Homoptera: Pseudocaccidae)
entomological mi9cro-technique. J Econ Entomol in Africa. Biocontrol Sci Technol 4:6169
39(5):655666 Neuenschwander P, Herren HR (1988) Biological control
Kairo MTK, Pollard GV, Peterkin DD, Lopez VF (2000) of the cassava mealybug, Phenacoccus manihoti, by
Biological control of the hibiscus mealybug, the exotic parasitoid Epidinocarsis lopezi in Africa.
Maconellicoccus hirsutus Green (Hemiptera: Philos Trans R Soc Lond B 318:319333
Pseudococcidiae) in the Caribbean. Integr Pest Manag Thao ML, Gullan PJ, Baumann P (2002) Secondary
Rev 5:241254 (-Proteobacteria) endosymbionts infect the primary
Koteja J (1974a) Comparative studies on the labium in the (-Proteobacteria) endosymbionts of mealybugs mul-
Coccinea (Homoptera). Zeszyty Naukowe Akademii tiple times and coevolve with their hosts. Appl Environ
Rolniczej w Krakowie 27:1162 Microbiol 68:31903197
74 M. Mani

Watson GW, Chandler LR (1999) Identication of mealy- Williams DJ (1985) Australian mealybugs. British
bugs in the Caribbean Region. CAB International, Museum (Natural History), London, 431p
Egham, 40 pp Williams DJ (1986) The identity and distribution of the
Westwood JO (1840) Synopsis of the genera of British genus Maconellicoccus Ezzat (Hemiptera:
Insects. [Appendix to]. An introduction to the modern Pseudococcidae) in Africa. Bull Entomol Res
classication of insects, founded on the natural habits 16:351357
and corresponding organisation of different families, Williams DJ, Granara de Willink MC (1992) Mealybugs
vol. 2, London, Longman, Orme, Brown, Green, and of Central and South America. CAB International,
Longmans, Paternoster-Row. 158 p Wallingford, 635 pp
Wilkey RF (1962) A simplied technique for clearing, Williams DJ (2004) Mealybugs of southern Asia. The
staining and permanently mounting small arthropods. Natural History Museum/Southdene Sdn. Bhd,
Ann Entomol Soc Am 55(5):606 London/Kaula Lumpur, 896 p
Williams DJ, Cox JM, Yaseen M (1981) The cassava Williams DJ, Granara de Willink MC (1992) Mealybugs
mealybug and its parasites in Paraguay and Bolivia. of Central and South America. CAB International,
Biocontrol News Inf 2:88 Wallingford, 635p
Molecular Identication
of Mealybugs 5
K.B. Rebijith, R. Asokan, and N.K. Krishna Kumar

Insects are the numerous life forms that have cap- has been a monumental task which calls for the
tured the attention of human beings since ancient availability of more specialists and funding. But
times. In the same context, proper classication with the dwindling interest in taxonomy and fund
and identication of life forms has been a chal- availability, the classication and identication
lenge, and a plausible method of classication of various life forms, particularly insects, has
was established by Carlous Linnaeus, a Swedish been a major challenge to the scientic commu-
botanist who published Systema Naturae in 1758. nity. With the advent of molecular biology and
However, the Linnaeus system of classication molecular tools, the identication of life forms,
was not based on evolutionary relationships including insects, has become quick, precise and
among the target groups. Later, Darwins The easy. The development of species-specic mark-
Origin of Species in 1859 changed the way life ers enables even a non-specialist to identify
forms were classied, where the identication, insects to the species level.
description and explanation of the diversity of
the organisms had come to be known as system-
atics. According to Mayr and Ashlock (1991), 5.1 Methods of Classication
systematics is the scientic study of the kinds and and Identication
diversity of organisms, and any and all relation-
ships among them; taxonomy, on the other hand, 5.1.1 Linnaean System
was the theory and practice of the classication
of organisms. It took 200 years for taxonomists Taxonomists assess the physical characteristics
to describe the 1.7 million species on the earth, that a set of species shares and selects the most
which is only 10 % of the total number of species representative species to be the type for each
estimated. In this context, identication of insects genus, and the most representative genus to be
the type of the family and so on. Individual speci-
mens are deposited in museums to serve as a ref-
K.B. Rebijith R. Asokan (*) erence for that species and genus. When new
Division of Biotechnology, Indian Institute of species are found with similar traits, they are cat-
Horticultural Research, Bangalore 560089, India
egorized as part of a known species as a new spe-
cies, or as a new genus, depending on how closely
N.K.K. Kumar
Indian Council for Agricultural Research,
the new specimens resemble the type. The reli-
New Delhi, India ance of types results in dramatic changes if a
e-mail: taxonomist re-evaluates a group and decides that

Springer India 2016 75

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_5
76 K.B. Rebijith et al.

some members do not belong and suggest that the ing to higher extinction rates and the introduction
group name must be changed. of invasive species of pests. Therefore, there is a
need for faster species identication and infor-
mation about their biodiversity for conserving
5.1.2 Cladistics them before they vanish from the face of the
earth. Undoubtedly, the contribution of morpho-
During the 1980s, another classication method logical taxonomy is enormous, but it also has
called cladistics, which is based on the evolution- some drawbacks, such as the following:
ary histories of organisms, was proposed. This
method is based on phylogeny, whereas the Incorrect identication due to phenotypic
Linnaean system is not. plasticity and genetic variability between dif-
ferent taxa of mealybugs
There are many morphologically cryptic taxa
5.1.3 Phylocode which are common in many groups
Morphological examination is time consum-
In this system, the genus name is removed, and ing and is often effective only for a particular
species name is shortened and hyphenated with life stage or gender (mostly in adult females in
their former genus name or given numeric case of mealybugs). As a result, many cannot
identication. be identied
Although modern interactive versions repre-
sent a major advance, the use of keys require
5.2 Shortfalls in Morphological high level of expertise that often lead to mis-
Identication identication (Hebert et al. 2003a)
Taxonomists have always looked for discon-
Mealybugs (Hemiptera: Pseudococcidae) are the tinuous character variations that could signal
major pests in a wide range of agricultural crops divergence between species. The debate on
as well as ornamental plants worldwide (Millar threshold values employing molecular identi-
2002; Miller et al. 2002, 2005). These sap- cation for interspecic divergence is also
sucking insects have been studied intensively for true in the case of morphology-based
decades because of the economic losses they identication.
cause to agriculture through direct physical dam- Early identication of new invasions is an
age to crop plants, as well as by vectoring many important aspect in preventing the spread.
plant pathogenic viruses, which in turn decreases Rapid and accurate identication of mealy-
yield quality (Meyer et al. 2008 and Nakaune bugs is not easily accomplished with conven-
et al. 2008). The family Pseudococcidae consists tional taxonomy. Taxonomy separation of
of more than 2000 described species in 270 gen- many species occurring together can be dif-
era (Downie and Gullan 2004). Current estimates cult, particularly for the nymphal stages that
suggest that the earth may have anywhere from are primarily involved
10 to more than 40 million species of organisms,
but only about 1.7 million of them have actually Hence, there is a need for an adjunct tool that
been described. It includes over 7,50,000 insects, facilitates rapid identication of species where
and it took 250 years for taxonomists to catego- molecular identication, popularly called DNA
rize all 1.7 million species, which comprise only barcoding, becomes handy. The concept of
10 % of the total species on earth (Hebert and DNA barcoding was proposed by Hebert et al.
Gregory 2005). Classifying the remaining 90 % (2003b, c) as a rapid and precise way for species
of the unidentied organisms will require more discrimination of a broad range of biological
time and expertise of taxonomists to complete specimens using a selected 658-bp fragment of
this monumental task. Economic development the 5 end of the mitochondrial cytochrome oxi-
and increased international commerce are lead- dase-I (mtCO-I) gene (Fig. 5.1).
5 Molecular Identication of Mealybugs 77

Fig. 5.1 (a) Organization of genes in mitochondrial and primer region (brown) with amino- and carboxy-
genome. (b) Arrangements of barcode region with mito- terminal spanning inside
chondrial membrane with barcode region (blue in colour)

5.2.1 Uses of DNA Barcoding cies whether abundant or rare, native or inva-
sive, engendering appreciation of biodiversity,
Works with fragments: Barcoding can identify locally and globally (Stoeckle et al. 2004).
a species from bits and pieces. When estab- Opens the way for an electronic hand-held
lished, barcoding will quickly identify unde- eld guide, the Life Barcoder: Barcoding links
sirable animal or plant material in processed biological identication to advancing frontiers
foodstuffs and detect commercial products in DNA sequencing, miniaturization in elec-
derived from regulated species (Stoeckle et al. tronics, and computerized information storage
2004). (Stoeckle et al. 2004).
Works for all stages of life: Barcoding can Demonstrates value of collections: Compiling
identify a species in its many forms, from eggs the library of barcodes begins with the multi-
and seed, through larvae and seedlings, to million specimens in museums, herbaria, zoos
adults and owers (Rebijith et al. 2012). and gardens and other biological repositories
Unmasks look-alikes: Barcoding can distin- (Stoeckle et al. 2004).
guish among species that look alike, uncover- Speeds up writing the encyclopaedia of life:
ing dangerous organisms masquerading as Compiling a library of barcodes linked to the
harmless ones, and enabling a more accurate vouchered specimens and their binomial
view of biodiversity (Asokan et al. 2011). names will enhance public access to biologi-
Reduces ambiguity: Written as a sequence of cal knowledge, helping to create an on-line
four discrete nucleotides CATG along a encyclopaedia of life on earth, with a webpage
uniform locality on genomes, a barcode of life for every species of plant and animal (Stoeckle
provides a digital identifying feature, supple- et al. 2004).
menting the more analog gradations of words,
shapes and colours (Stoeckle et al. 2004). The core idea of barcoding is based on the fact
Democratizes access: A standardized library that short pieces of DNA vary only to very a
of barcodes will empower many more people minor degree within the species, and that the
to call by name the species around them. It variation is much less between different species.
will make possible the identication of spe- Therefore, a threshold value of variation could be
78 K.B. Rebijith et al.

characterized for each taxonomic group (212 mitochondrial, is unlikely to yield data that are
%), above which groups of individuals do not balanced, universally acceptable, or sufcient in
belong to the same species, but form supra- taxonomic scope to recognize many species lin-
species taxon. Therefore, unknown individuals eages (Rubinoff 2006). Mitochondrial cyto-
could be assigned to a species level. chrome c oxidase subunit I (mtCO-I) gene
sequence is suitable for this role because its
mutation rate is often fast enough to distinguish
5.3 Targets for Molecular closely related species, and also because its
Identication sequence is conserved among conspecics and a
lack of recombination. mtCO-I sequence differ-
5.3.1 Mitochondrial DNA ences are too small to be detected between closely
related species; more than 2 % sequence diver-
Mitochondrial (mt) DNA (Fig. 5.2) has a long gence has been detected between such organ-
history of use at the species level; recent analyses isms, proving the barcode effective. However,
suggest that the use of a single gene, particularly the rate of evolution of cox1 is very slow.

Fig. 5.2 Flowchart showing steps in DNA barcoding of mealybugs, from collection to sequence deposition in iBOL
5 Molecular Identication of Mealybugs 79

5.4 Advantages of Using phenol:chloroform method and (d) salting out

Mitochondrial Genome method.

Haploid mode of inheritance, and it supports Direct Buffer Method

less recombination A single insect can be crushed in 50200 L
Mitochondrial genome does not have introns YNES (50 mM TrisHCI, pH 7.5, 0.4 M NaCI,
Universal primers are robust, which can 20 mM EDTA, 0.5 % SDS), STE (0.1 M NaCI,
amplify 5 end in most of the animals, includ- 10 mM Tris, pH 8.61 mM EDTA), GES (0.1 M
ing insects glycine, pH 9, 50 mM NaCI, 1 mM EDTA, 1 %
Rapid evolution allows the discrimination of -mercaptoethanol, 0.5 % Triton X-100) or
not only closely related species but also phylo- CTAB (100 mM TrisHCL, pH8,1.4 M NaCI, 20
graphic groups within a single species mM EDTA, 2%CTAB, 0.2 % -mercaptoethanol)
In animal mitochondrial genome, the 13 pro- buffer. The sample is to be incubated at 94 C for
tein coding genes are better targets because of 12 min, with the cell debris to be precipitated by
rare insertions and deletions (indels) spinning it at 13,000 rpm for 1 min. The extracted
By identifying amino acid substitution pat- DNA is to be stored at 20 C.
terns of mtCO1, it is possible to assign any
undened organisms to a higher taxonomic Spot-PCR Method
group before examining nucleotide substitu- A single insect should be crushed on a positively
tions to determine its species identity charged nylon membrane soaked in a 50-mM
NaOH and 2.5-mM EDTA solution, and then
allowed to dry. A small portion (ca. 3 mm2) of the
5.5 Collection spotted membrane is to be cut out and placed in
and Morphological 1050 L TNES, STE, GES or CTAB buffer
Identication (described above). The sample can then be incu-
bated at 95 C for 10 min and cooled on ice.
Mealybug specimens can be collected in 95 % Extracted DNA can be stored at 20 C.
ethanol and kept at 80 C (deep freezer) until
further work. Morphological identication can Phenol/Chloroform Method
be carried out by a taxonomist. Whenever possi- DNA from a single insect can be extracted using
ble, it is better to analyse at least three specimens the modication of a general procedure for
collected from each of the host/locality for extraction with phenol (Sambrook et al. 1989;
reproducibility. Sambrook and Russell 2001). The insect is to be
crushed and incubated at 40 C in 0.6 mg/mL
Proteinase K and 300 L TNES buffer for 418
5.5.1 Genomic DNA Isolation h. DNA can then be puried by washing with
organic solvents: once with a chloroform:isoamyl
Total genomic DNA can be extracted from indi- mix (24:1 v/v); once with a chloroform:phenol
vidual mealybugs using a non-destructive method mix (1:1 v/v) and once with chloroform only.
(Hajibabaei et al. 2006), while voucher speci- DNA can then be precipitated with absolute etha-
mens are required to be mounted on glass slides nol. Extracted DNA can be stored at 20 C.
and deposited with any of the National Insect
Repository such as the National Pusa Collection Salting-Out Method
(NPC) or the Indian Agricultural Research DNA from a single whole insect can be extracted
Institute (IARI), Delhi. Various DNA isolation using the protocol of Sunnucks and Hales (1996)
protocols are available, namely (a) direct TNES with minor adjustments, including the following:
buffer method, (b) spot-PCR method, (c) the insect can be incubated at 40 C in 0.6 mg/mL
80 K.B. Rebijith et al.

Proteinase K and TNES buffer; and the samples DNA Analyzer; Applied Biosystems, USA) using
can be left for at least 1 h at 20 C during pre- PCR specic primers, both in forward and reverse
cipitation of the DNA with absolute ethanol. directions. Homology search and sequence align-
Extracted DNA can be stored at 20 C. ment can be performed employing the NCBI-
BLAST ( and
BioEdit version (Hall 1999), respectively.
5.5.2 Polymerase Chain Reaction All the sequences generated in the respective
studies need to be deposited in the NCBI-
Polymerase chain reaction (PCR) was developed GenBank and the Barcode of Life Data systems
by Kary B. Mullis (Mullis and Faloona 1987) and (BOLD) (Table 5.2).
has radically changed molecular research and
diagnostics (Caterino et al. 2000). PCR involves
the in vitro synthesis of large amounts of DNA 5.6 Nuclear Copies
copies from a single starting molecule and of Mitochondrial Genes
employs short single strands of DNA (1830
nucleotides) called oligomers or primers (Table There is a possibility that a pseudogene is being
5.1) to select a region of specic interest from the amplied if the study encounters the following
DNA. Once the primers are annealed to the DNA, anomalies (Zhang and Hewitt 1996):
Taq DNA polymerase builds a complementary
strand extending from the primer by incorporat- More than one bands, or different bands, are
ing free deoxynucleoside triphosphate (dNTP: constantly produced during PCR
base + deoxyribose sugar + phosphate) molecules amplication.
in the reaction mix. Two primers that anneal on Background peaks or sequence ambiguities
complementary strands are used, with the Taq are constantly found when sequencing.
extending the region between them. The reaction The DNA sequence contains data which will
mixture is cycled between different temperature unexpectedly change the polymerase transla-
optima for the different stages of reaction of tion of the sequence, such as unusual frame-
denaturation, annealing and elongation. This pro- shifts, insertion/deletion or stop codons.
cess is repeated in a number of cycles (usually The DNA sequence is particularly more diver-
3040), and the DNA thus produced increases gent than expected.
exponentially (Saccaggi 2006). Phylogenetic analysis results in unusual,
unexplained or contradictory tree topology.

5.5.3 Sequence Analyses In the recent past, DNA barcoding has gained
and Submission importance in the species diagnosis of animal
species, but has some difculty with certain
The amplied products can be eluted using an insects. This is probably due to its inconsistency
extraction kit according to the manufacturers in amplifying the 5- mtCOI region; however, a
protocol, and the sequencing can be done in an total of 178 mtCOI sequences for 29 mealybug
automated sequencer (ABI prism 3730 XL species are available with the NCBI-GenBank.

Table 5.1 Primers employed in DNA barcoding of mealybugs

mtCO-I Sequence Amplicon Size (bp) Reference
LCO-1490 5-GGTCAACAAATCATAAAGATATTGG-3 658 bp Folmer et al. (1994)
PcoF1 5- CCTTCAACTAATCATAAAAATATYAG-3 649 bp Park et al. (2010a)
5 Molecular Identication of Mealybugs 81

Table 5.2 Maximum composite likelihood estimate of and biotypes (Shufran et al. 2000). In this regard,
the pattern of nucleotide substitution from 29 species of
sequence analyses revealed that the specimen of
a single species, namely Planococcus cus,
A T C G Crisicoccus matsumotoi, Phenacoccus solani
A - 10.58 2.19 2.4 and P. aceris, from various geographic regions
T 8.03 6.15 1.07
and hosts often showed substantial genetic differ-
C 8.03 29.68 1.07
ence, possibly reecting cryptic species over-
G 18.04 10.58 2.19
looked by current taxonomy classication (Park
The nucleotide frequencies are 0.367 (A), 0.484 (T/U),
et al. 2011). However, further studies are required
0.1 (C) and 0.049 (G). The transition/transversion rate
ratios are k1 = 2.247 (purines) and k2 = 2.805 (pyrimidines). in this direction to clarify these potential cases of
The overall transition/transversion bias is R = 0.443, cryptic mealybug species (Fig. 5.4).
where R = [A*G*k1 + T*C*k2]/[(A + G)*(T + C)]. Codon
positions included were 1st + 2nd + 3rd + Noncoding
5.7 Limitations of DNA
Barcoding Employing mtCOI
All the above species could be clearly differenti-
ated on the basis of the 5- mtCOI barcode (Fig. Following are the limitations of DNA barcoding
5.3), which is a valuable tool for the identica- employing mtCOI:
tion of these serious insect pests, an approach
complementing classical taxonomy. An insight Limitations in resolving species at species
into the sequence analyses revealed that the G.C boundaries in some groups where nuclear
content in the barcode region is very low (14.9 ribosomal regions are suitable.
%) and is the lowest from any insect species, mtCOI does not show much variation in
which is in total contrast to other lineages (3353 plants, except for some algae.
%) (Min and Hickey 2007; Park et al. 2011). Introgression: mtCOI is largely maternally
Interestingly, the low G.C frequency is more pre- inherited, and usually as a single copy. Hence,
dominant at the third codon (wobble position), it has one fourth the population size of other
than the rst and second position. Among various nuclear genes, has a different inheritance pat-
life forms, the G.C content (12.6 %) for tern and is more sensitive than nuclear genes
Atrococcus paludinus is the lowest value, which to population bottlenecks. mtDNA introgres-
is even lower than bacterial genomes whose G.C sion confounds the boundaries between other-
content is in the range of 1775 %. The lowest wise distinct lineages; such introgression
G.C content (1733 %) occurs in bacterial spe- between species could lead to inaccurate
cies with small genome sizes, especially the identications.
endosymbionts of insects, such as aphids Maternal inheritance: The full effect of mater-
(Andersson and Kurland 1998; Moran et al. nal inheritance on rates of molecular diver-
2008). The lower G.C content in insects such as gence in mtDNA is not predictable, and
scales and mealybugs, feeding on plant sap, a diet therefore the failure rate of DNA barcoding is
which is very decient in organic nitrogen, pos- also unpredictable. mtDNA is inherited mater-
sibly can be explained as an evolutionary adapta- nally, but not in bivalve molluscs which dis-
tion to less nitrogen and relatively less nitrogen is play double unpatented mtDNA inheritance. It
required for A.T than G.C pair. is also evident in a wide range of the taxa
DNA barcoding can be used as an acceptable infrequent paternal inheritance.
system for molecular identication of species in Low recombination: The general absence of
its distinct life stages and forms (Foottit et al. recombination will lead to the persistence of
2010; Rebijith et al. 2012), host-associated population structure long after the barriers
genetic differences (Brunner et al. 2004), dis- which created the structures are removed and
crimination of cryptic species (Smith et al. 2006) gene ow is restored. Therefore, it is not pos-
82 K.B. Rebijith et al.

Planococcus kraunhiae (12)
Planococcus lilacinus (6)
Planococcus ficus (4)

99 JF965419_Planococcus minor
Planococcus citri (9)
Crisicoccus pini (2)
Atrococcus paludinus (3)
Pseudococcus calceolariae (7)
Dysmicoccus lepelleyi (7)
65 Pseudococcus cryptus (5)
Pseudococcus com stocki (9)
Paracoccus marginatus (7)
Balanococcus takahashii (2)
Crisicoccus matsumotoi (19)
Pseudococcus jackbeardsleyi (8)
Pseudococcus viburni (3)
Dysmicoccus brevipes (3)
Dysmicoccus neobrevipes (15)
Maconellicoccus hirsutus (4)
Palmicultor lumpurensis (3)
Ferrisia virgata (2)
Ferrisia malvastra (4)
HM474183_Heliococcus puerariae
Dysmicoccus wistariae (2)
Pseudococcus longispinus (12)
Phenacoccus aceris (11)
Heliococcus kurilensis (7)
HM474263_Phenacoccus avenae
Phenacoccus solani (9)


Fig. 5.3 NJ tree with bootstrap support (1000 replicates) matsumotoi, Phenacoccus solani and P. aceris showing
showing clusters of species for mtCOI sequences. Distinct two distinct groups with >90 % bootstrap support. The
clades for 29 species of aphids can be seen in the gure, in numbers indicated in brackets represent the individuals
which four species, namely Planococcus cus, Crisicoccus analysed in the corresponding species

sible to estimate species boundaries which tent mutation rate, such as the proposed 23 %
would have been estimated from a broader divergence to correlate with species limit on a
data set. consistent basis. Speciation, uniquely driven
Mutation rate: For the DNA barcode to be by changes in mtDNA or speciation event,
used as standalone, there should be a consis- necessarily alters the mtDNA haplotypes.
5 Molecular Identication of Mealybugs 83

Fig. 5.4 Neighbour joining (NJ) showing intra-specic variation in the barcode region for four species of mealybugs,
namely Planococcus cus (a), Phenacoccus solani (b), Crisicoccus matsumotoi (c) and P. aceris (d)

Heteroplasmy: This refers to the classical barcoding initiative of the animal kingdom will
view of mitochondria functionally haploid produce about 100 million sequences and will be
with multiple identical copies. However, sin- available through GenBank.
gle nucleotide differences are common in An international database called BOLD
some species and are also abundant in some, (Barcode of Life Data system) organizes the
especially at the restriction sites. sequence data on species identication, which
Compounding genetic factors: Coinheritance was initially developed as an informatics work
factors that bias single mitochondrial inheri- bench for a single, high-volume DNA barcode
tance and most obvious are (a) mitochondrial facility. Later, the same has been selected by
selection either on the barcoding gene itself or the Canadian Barcode of Life Network (www.
on the other linked genes; (b) cytoplasmically to barcode all the eukaryotic life of
inherited bacteria like Wolbachia and some Canada, and subsequently, it has been adopted
Rickettsia which alter the inheritance factors by major barcode communities like birds,
(Rubinoff et al. 2006). shes, lepidoptera, etc. BOLD provides an inte-
Identication depends on the intra- and inter- grated bioinformatics platform that supports all
specic genetic variations. phases of analytical pathway from specimen
Difcult to resolve, recently diverged species collection to a tightly validated barcode library.
that arose through hybridization. It also provides a vehicle for collaboration
No single gene is conserved in all domains of across research communities by coupling exi-
life and exhibit enough sequence divergence ble security and data entry features with web
for species discrimination. based delivery. A copy of all sequences in
BOLD is also sent to NCBI, DDBJ, and EMBL
There are about 52 million sequence records as soon as the results are ready for public
available currently, and it is expected that the release.
84 K.B. Rebijith et al.

5.8 Other Targets for Molecular In addition to the above reterotransposons, R1

Identication of Insects and R2 have been in the 28S rRNA genes of most
insects, are associated with arthropods, and are
5.8.1 Ribosomal DNA usually precisely located at the same nucleotide
position within the 28S rRNA gene. Most of the
Ribosomes are the major components of cells R2 elements are located about 74 bp upstream
that are involved in translating the mRNA into from the site of R1 insertions. R1 and R2 do not
proteins. Ribosomes consist of both proteins have long terminal repeats and block the produc-
and RNAs. The ribosomal RNA (rRNA) regions tion of functional rRNA, since there are many
that are conserved and more variable regions rRNA genes, and R2 are kept from invading by
can serve as both slow and fast clocks in identi- miRNA/siRNA. Usually, R1 and R2 do not have
fying and unravelling the molecular phylogeny. accumulated mutations that would make them
In eukaryotes (including insects), the genes inactive.
encoding both 18S and 28S rRNA are clustered
as tandem repeats in the nucleolus; in most ani-
mals, there are 100500 copies of rDNA in the 5.8.2 Satellite DNA
nuclear genome in tandemly repeated transcrip-
tion units. The repeated transcription unit is Satellite DNA may consist of a large fraction of
composed of a leader promoter region known as the total DNA in an insect. Microsatellites are
external transcribed spacer region (ETS), 18S usually species specic, and evolve at very high
rDNA coding region, internal transcribed spacer rates. Satellite DNA can also be used for species
region (ITS), 28S rDNA coding region and an identication and analysis of populations.
internal non-coding transcribed spacer region
(IGS). In addition to the above, R1 and R2 retro
transposable elements are found in specic 5.8.3 Nuclear Protein Coding Genes
locations (Fig. 5.5).
Different portions of the repeated transcrip- A variety of protein coding loci have been used
tion units evolve at different rates in the nuclear in molecular systematics, and some of them are
genome; a higher degree of polymorphism is listed below:
found in the non-coding segments (IGS, ITS,
ETS), and the most variable part of the repeated 1. alpha amylase 2. acetyl choline esterase 3.
unit is IGS, which contains reiterated sub-repeats actin 4. alcohol dehydrogenase 5. arylphorin
ranging from 50 to several hundred base pairs in 6. cecropin 7. chorin 8. dopa carbaxylase 9.
length. The coding regions of the repeated unit elongation factor 1 alpha 10. esterase 11. glyc-
change relatively less and can be used for sys- erol 3 phosphate 12. glycerol 6 phosphate
tematic studies of higher taxa or for ancient lin- dehydrogenase 13. guanylate cyclase 14. glo-
eages. Ribosomal RNA genes undergo concerted bin family genes 15. histones 1 and 4 16.
evolution so that the sequence similarity of the hunch back 17. kruppel 18. luciferase 19.
members of an RNA family is expected to be lysozyme intron 20. myosin alkali light
greater within species than between species. chain intron 21. nullo 22. opsin 23. period 24.

18S 28S

Fig. 5.5 Gene organization of ribosomal genes

5 Molecular Identication of Mealybugs 85

phosphogluco isomerase 25. phosphoenol RAPD data clearly separated the species into
pyruate carboxy kinase 26. prune 27. copper, two groups (Serce et al. 2007).
zinc superoxide dismutase 28. sodium channel 2. Seven species of mealybugs (Ps maritimus,
para locus I 29. snail 30. timeless 31. triose- Ps.vibruni. Ps.longispinus, Ps.calceolariae,
phosphate isomerase 32. vestigial 33. white Pl.cus, Pl.citri, Ferrisia gilli Gullan) were
34. wingless 35. xanthine dehydrogenase 36. identied using a Multiplex PCR based on the
yolk protein 1 and 2 37. zeste. mitochondrial cytochrome oxidase subunit
gene (Daane et al. 2011).
3. There was a slight difference in morphologi-
5.9 Limitations cal characters in the populations of
Planococcus cus, indicating that there are
May be heterozygous and present in low copy two different populations of the same species
numbers. in Tunisian vineyards. Likewise, in the molec-
Many genes contain large introns that makes it ular analyses, two separate clades were
difcult to amplify more than one exon. revealed in the neighbour-joining phyloge-
Many single-copy loci are actually are present netic tree, supporting the morphological stud-
in more than one copy. ies and suggesting there are two distinct
Pseudogenes may create problem if compari- populations of grape vine in Tunisia, which
sons are made inadvertently. might be two different biotypes (Mansour
et al. 2012).
Even with all the limitations, the molecular
identication of insects employing mtCOI is
gaining momentum, and as of now it can be an
effective adjunct tool for the integrated taxon- References
omy. Many barcoding initiatives are beginning to
take shape, such as the recent initiative on Andersson SG, Kurland CG (1998) Reductive evolution
of resident genomes. Trends Microbiol 6:263268
Barcoding of butteries of India funded by the Asokan R, Rebijith KB, Singh SK, Sidhu AS, Siddharthan
Department of Biotechnology. With the increase S, Karanth PK, Ellango R, Ramamurthy VV (2011)
in international trade on agricultural produces Molecular identication and phylogeny of Bactrocera
where the danger of introduction of invasive spe- Species (Diptera: Tephritidae). Fla Entomol
cies looms large, DNA barcoding is going to play Brunner PC, Chatzivassilious EK, Katis NI, Frey JE
a vital role in the quick identication of insect- (2004) Host associated genetic differentiation in
pests at the port of entry. As ambitiously envis- Thrips tabaci (Insecta: Thysanoptera), as determined
aged, the development and deployment of the from mtDNA sequence data. Heredity 93:364370
Caterino MS, Cho S, Sperling FAH (2000) The current
hand-held sequencer, which is supported by the state of insect molecular systematics: a thriving tower
global networked database, is going to revolu- of Babel. Ann Rev Entomol 45:154
tionize the way we identify insects that are Daane KM, Middleton MC, Sforza R, Cooper ML, Walton
already described, along with the new ones. VA, Walsh DB, Zaviezo T, Almeida PP (2011)
Development of a multiplex PCR for identication of
vineyard mealybugs. Mol Ecol Evol
5.10 Applications Downie DA, Gullan PJ (2004) Phylogenetic analysis of
mealybugs (Hemiptera: Coccoidea: Pseudococcidae)
based on DNA sequences from three nuclear genes,
1. The relationship of six mealybug species (Pl. and a review of the higher classication. Syst Entomol
citri, Pl.cus, P.ovae, Ps.longispinus, Ps.vibruni, 29:238259
Ph.aceris) was studied using randomly amplied Folmer O, Black M, Hoe W, Lutz R, Vrijenhoek R (1994)
polymorphic DNA-polymerase chain reaction DNA primers for amplication of mitochondrial cyto-
chrome c oxidase I from diverse metazoan inverte-
(RAPD-PCR) in Turkey. Cluster analyses of brates. Mol Mar Biol Biotechnol 3:294299
86 K.B. Rebijith et al.

Foottit RG, Maw HEL, Pike KS, Miller RH (2010) The Park DS, Suh SJ, Oh HW, Heber PDN (2010) Recovery of
identity of Pentalonia nigronervosa and P. caladii van the mitochondrial COI barcode region in diverse
der Goot (Hemiptera: Aphididae) based on molecular Hexapoda through tRNA-based primers. BMC
and morphometric analysis. Zootaxa 2358:2538 Genomics 11:423
Hajibabaei M, Janzen DH, Burns JM, Hallwachs W, Park DS, Suh SJ, Hebert PDN, Oh HW, Hong KJ (2011)
Hebert PDN (2006) DNA barcodes distinguish species DNA barcodes for two scale insect families, mealy-
of tropical Lepidoptera. Proc Natl Acad Sci U S A bugs (Hemiptera: Pseudococcidea) and armored scales
103:968971 (Hemiptera: Diaspididae). Bull Entomol Res
Hall TA (1999) BioEdit: a user-friendly biological sequence 101:429434
alignment editor and analysis program for Windows Rebijith KB, Asokan R, Krishna Kumar NK, Srikumar
95/98/NT. Nucleic Acids Symp Ser 41:9598 KK, Ramamurthy VV, Shivarama Bhat P (2012) DNA
Hebert PDN, Gregory TR (2005) The promise of DNA barcoding and development of species-specic mark-
barcoding for taxonomy. Syst Biol 54:852859 ers for the identication of Tea mosquito bugs
Hebert PDW, Cywinska A, Ball SL, deWaard JR (2003a) (Miridae: Heteroptera) in India. Environ Entomol
Biological identication through DNA barcodes. Proc 41:12391245
Roy Soc Lond B 270:313321 Rubinoff D (2006) Utility of mitochondrial DNA bar-
Hebert PDN, Cywinska A, Ball SL, DeWaard JR (2003b) codes in species conservation. Conserv Biol
Biological identications through DNA barcodes. 20:10261033
Proc Roy Soc B Biol Sci 270:313322 Rubinoff D, Cameron S, Will K (2006) A genomic
Hebert PDN, Ratnasignham S, deWaard JR (2003c) perspective on the shortcomings of mitochondrial
Barcoding animal life: cytochrome c oxidase subunit 1 DNA for Barcoding identification. J Hered 97:
divergences among closely related species. Proc Roy 581594
Soc Lond Ser B 270(Suppl. 1):S96S99 Saccaggi DC (2006) Development of molecular tech-
Mansour R, Cavalleri V, Mazzeo G, Lebdi KG, Russo A niques to identify mealybugs (Hemiptera:
(2012) A morphological and molecular characteriza- Pseudococcidae) of importance on grapevine in South
tion of vine populations (Hemiptera, Pseudococcidae) Africa. University of Pretoria, Pretoria
from Tunisia. J Entomol Acarol Res 44(e5):2427 Sambrook J, Russell M (2001) Molecular cloning: a labo-
Mayr E, Ashlock PD (1991) Principles of systematic zool- ratory manual, 3rd edn. Cold Spring Harbor Laboratory
ogy, 2nd edn. McGraw-Hill, New York Press, New York
Meyer JB, Kasdorf GGF, Nel LH, Pietersen G (2008) Sambrook J, Fritsch EF, Maniatis T (1989) Molecular
Transmission of activated-episomal banana streak ol cloning: a laboratory manual, 2nd edn. Cold Spring
(badna) virus (bsolv) to cv. Williams banana (musa sp.) Harbor Laboratory Press, New York, 1659p
by three mealybug species. Plant Dis 92:11581163 Serce CU, Kaydan MB, Kilincer AN, Ertunce F (2007)
Millar IM (2002) Mealybug genera (Hemiptera: Investigation of mealybug (Hemiptera: Coccoidea:
Pseudococcidae) of South Africa: identication and Pseudicoccidae) species from Turkey by
review. Afr Entomol 10:185233 RAPD. Phytoparasitica 35(3):232238
Miller DR, Miller GL, Watson GW (2002) Invasive spe- Shufran KA, Burd JD, Anstead JA, Lushai G (2000)
cies of mealybugs (Hemiptera: Pseudococcidae) and Mitochondrial DNA sequencedivergence among
their threat to US agriculture. Proc Entomol Soc Wash greenbug (Homoptera: Aphididae) biotypes: evidence
104:825836 for hostadapted races. Insect Mol Biol 9:179184
Miller DR, Miller GL, Hodges GS, Davidson JA (2005) Smith MA, Woodley NE, Janzen DH, Hallwachs W,
Introduced scale insects (Hemiptera: Coccoidea) of Hebert PDN (2006) DNA barcodes reveal cryptic
the United States and their impact on us agriculture. host-specicity within the presumed polyphagous
Proc Entomol Soc Wash 107:123158 members of a genus of parasitoid ies (Diptera:
Min XJ, Hickey DA (2007) DNA barcodes provide a Tachinidae). Proc Natl Acad Sci U S A
quick preview of mitochondrial genome composition. 103:36573662
PLoS ONE 2(3), e325 Stoeckle MY, Zemlak TS, Francis CM (2004)
Moran NA, McCutcheon JP, Nakabachi A (2008) Identication of birds through DNA barcodes. PLoS
Genomics and evolution of heritable bacterial symbi- Biol 2(10), e312
onts. Ann Rev Genet 42:165190 Sunnucks P, Hales DF (1996) Numerous transposed
Mullis KB, Faloona FA (1987) Specic synthesis of DNA sequences of mitochondrial cytochrome oxidase I-II in
in vitro via a polymerase-catalyzed chain reaction. aphids of the genus Sitobion (Hemiptera: Aphididae).
Methods Enzymol 155:335350 Mol Biol Evol 13:510524
Nakaune R, Toda S, Mochizuki M, Nakano M (2008) Zhang DX, Hewitt GD (1996) Nuclear integrations: chal-
Identication and characterization of a new vitivirus lenges for mitochondrial DNA markers. Tree
from grapevine. Arch Virol 153:18271832 11:247251
M. Mani and C. Shivaraju

A few generalizations on the biology of mealy- citri (Risso). To attract adult males, the females
bugs are derived primarily from the detailed stud- emit a sex pheromone. Female mealybugs mate
ies of the work previously done on common multiple times and the number of times they mate
mealybug species. There are slight variations in also affects the egg production. Parthenogenetic
the biology of mealybugs among the species. reproduction is also observed in many mealybug
species, while in some others, reproduction is by
both sexual and parthenogenetic means.
6.1 Reproduction Most mealybug species reproduce sexually, as
well as lay eggs. However, some species such as
The mature or gravid adult female begins to grow in Phenacoccus solani Ferris, Phenacoccus parvus
size as the ovaries develop, ending at about 45 mm Morrison and Ferrisia malvastra (McDaniel)
in length and far less dorso-ventrally attened. The reproduce parthenogenically and others, for exam-
adult male is about 1.5 mm in length, with long ple, Pseudococcus longispinus (Targioni Tozzetti)
wings, a brown-coloured body and two multi-seg- and Antonina graminis (Maskell) are ovovivipa-
mented antennae that are about half the length of rous. Two different genetic systems may be found
the body. Mealybugs have the lecanoid type of the in mealybugs; the more common corresponds to a
paternal genome elimination system, where both particular type of haplodiploidy known as paternal
sexes develop from fertilized eggs (i.e., diploidy), genome elimination in which both males and
but during the early stage of development of the females develop from fertilized eggs. The male
male, the paternal half is deactivated through het- develops from a zygote containing one haploid
erochromatinization. This system suggests that the genome from his mother and one haploid genome
females would produce a male-biased sex ratio from his father, but only the maternal genome is
when alone and a more female-biased sex ratio transmitted to the offspring via the sperm, because
when grouped with other females. Mealybug repro- the set of chromosomes of paternal origin becomes
duction can be quite variable. For some mealybugs, heterochromatic and genetically inactive. Male
mating is probably necessary, although facultative mealybugs are thus functionally haploid, owing to
parthenogenesis has been reported for Planococcus heterochromatization (parahaploidy). The other
genetic system is thelytokous parthenogenesis, in
which there are no males and therefore no mating
M. Mani (*) C. Shivaraju
occurs. There are no sex chromosomes in mealy-
Indian Institute of Horticultural Research,
Bangalore 560089, India bugs; sex is probably determined by a functional
e-mail: haploidy/diploidy mechanism, which seems to be

Springer India 2016 87

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_6
88 M. Mani and C. Shivaraju

dependent on the behaviour of a set of chromo- The male is holometabolic and develops
somes and not on a single chromosome. If hetero- through four stages, egg, larva (two nymphal
chromatization of an entire set of chromosomes instars), pupa and adult, while the female is
takes place during the cleavage stage of embryo- hemimetabolic and develops through three
genesis, the embryo will develop into a male, or stages, egg, larva (three nymphal instars) and
otherwise into a female. Spermatogenesis is char- adult.
acterized by inverse meiosis and the absence of
chromosome pairing and genetic recombination
where the genome of the mother determines the 6.1.1 Oviposition
heterochromatization of the inherited paternal
chromosomes in mealybug embryos. According Mealybugs may be oviparous, viviparous or ovo-
to this model, heterochromatization is controlled viparous. Although variable, the pre-oviposition
by a maternal factor, with the maternally derived period is 45 days in general. In most of the
chromosomes imprinted so that they do not suffer mealybugs like Pseudococcus longispinus,
the fate of the male chromosome. Sex determina- Ferrisia gilli Gullan, Dysmicoccus brevipes
tion in mealybugs, and consequently the sex ratio, (Cockerell) and Heliococcus bohemicus Sulc.,
is known to be inuenced by temperature and the eggs are laid by the adult female among the la-
age of the mother. The effect of the temperature or mentous secretion of the ovisac formed by the
the age of the mother on the sex ratio of the off- pores on the adult's body. Wax secreted by the
spring is attributed to a change in the ratio between numerous pores and ducts around the ovi-
the numbers of oocytes with and without the positional opening plays an important role in
maternal factor. forming a waxy sac around the laid eggs. The
6 Biology 89

ovisacs are somewhat variable in their structure, depending on the species, environmental condi-
depending upon the species of the mealybug. tions and food supply. It has been reported rang-
Several types of ovisacs have been recorded, ing from about 50 to over 800. In the absence of
varying from one covering the entire female adult males, the virgin females of Planococcus
body, to one covering only half or perhaps the minor (Maskell) do not produce eggs.
last two abdominal segments, to one which is
entirely ventral. These ovisacs are normally
deposited on the shoots, fruits, owers, leaves, 6.1.2 Incubation
underneath the bark and the cracks and crevices
of the plant stem and arms. The eggs hatch between 4 and 10 days, depend-
The eggs are oval and can be seen with the ing on the temperature and humidity. Hatching
naked eye, while the colour of the eggs varies percentage ranges from 80 to 90 %.
with the species. The normal oviposition period
of female mealybugs is 68 days, but it differs
depending upon the species and climatic condi- 6.1.3 Nymph
tions. They are in close proximity in the ovisac.
Female mealybugs are capable of mating multi- Mealybugs generally have three larval instars for
ple times on the same day and the female repro- females and four for males. Each of these stages
ductive output is unaffected by multiple resembles the previous one, except for an increase
copulations. As many as 600 eggs can be laid by in size and the amount of wax secreted. Usually,
one female, but the number of eggs varies accord- immature males are slightly longer and more
ing to the mealybug and the host species. Freshly slender than females.
laid eggs vary in colour in different species, for
example, the eggs are orange in case of
Maconellicoccus hirsutus (Green), violet in case 6.1.4 First-Instar Nymph (Both
of Nipaecoccus viridis (Newstead), yellow in Sexes)
case of most of the mealybugs like Planococcus
citri (Risso). However, the colour changes The eggs hatch into rst-instar nymphs or crawl-
slightly before hatching, and the size also varies ers and are vulnerable to insecticidal applica-
in different species. In the case of M. hirsutus, the tions. This stage usually has proportionally very
eggs are 0.340.38 mm in length and the width large legs and antennae compared with other
ranges from 0.17 to 0.20 mm. Most of the mealy- instars and often there are fewer antennal seg-
bugs are oviparous and they lay eggs in the ovi- ments than in the adult. This crawler is often
sac. But some mealybugs are ovoviviparous quite mobile and usually migrates to other hosts,
(depositing live rst instars); for example, or at least to diverse areas of the parent host.
Dysmicoccus brevipes (Cockerell) bears live There is no reliable character to distinguish
young, producing as many as 908 crawlers. These between the male and female at this stage. The
ovoviviparous females produce little or no ovisac mean duration of the rst instar is about 67
and apparently shield their young for a short time days; there is not much variation between male
by covering them with their abdomen. This char- and female instars, but it can vary under different
acter is particularly true of Puto, a genus which, conditions of temperature and humidity. When
for the most part, is ovoviviparous. Planococcus viewed from above, it seems elongate oval in
lilacinus (Cockerell) also lays the crawlers shape, but is extremely at from the side. The
directly, while Ferrisia virgata (Cockerell) lays rst-instar nymph is often free from the waxy
eggs which hatch immediately after laying. The coating which usually develops at the later stages
number of offspring produced per female varies of growth.
90 M. Mani and C. Shivaraju

6.1.5 Second-Instar Nymph (Both instar male is about 1 day, but it again varies
Sexes) according to temperature and humidity condi-
tions for different species.
The second-instar nymph emerges through a slit
in the medio-dorsum of the head and thorax of
the rst-instar skin. The legs and antennae are 6.1.7 Fourth-Instar Male
still proportionally larger compared to the adult
body and often there are fewer antennal segments The fourth instar of the male is produced in a
than in the adult. During this stage, it is possible cocoon and is known as the pupa. The third skin
to differentiate between the sexes, for by the end that is shed is again shoved to the back of the
of this instar, the males produce a lamentous sac cocoon. This instar differs from the previously
or cocoon over their bodies. The rostrum of the mentioned one; it has two longer, backwardly
male is lost after the rst moult, making the rec- directed wing pads, more antennal segments (ten-
ognition of the second-instar male quite simple. jointed, normally the same as the adult) with a
The second nymphal stage of the female is char- few pointed setae and three pairs of eyes. At one
acterized by the presence of six jointed antennae, point between this instar and the next, a break in
four pairs of cerarii in the abdominal segments the posterior part of the cocoon is formed and the
VIIX and the oral rim ducts are restricted to the fourth shed skin is pushed outside. The duration
dorsum. In the second stage, the male only has of the fourth instar/pupa is about 6 days, but it
one pair of, rarely two pairs of, cerarii and tubular again varies under different conditions of tem-
ducts of oral collar type both on the dorsum and perature and humidity.
the venter. Mean duration of the second instar is
about 67 days, but not much variation is seen
between male and female instars, though it can 6.1.8 Adult Female
be variable under different conditions of temper-
ature and humidity. The adult female is almost similar to the third-
instar female nymph. The third-instar female has
seven-jointed antennae and ve pairs of cerarii in
6.1.6 Third-Instar Nymph (Both the abdominal segments VIX, but the adult
Sexes) female has nine-jointed antennae, six pairs of
cerarii in the abdominal segments IVIX., valvu-
The second-instar skin is shed in the same man- lar opening and multilocular disc pores in the
ner as the rst, producing the third-instar nymph. venter. The fourth-instar female emerges in the
In female specimens, these instars begin to take usual manner to become an adult. The female
the normal shape of the adult. Legs and antennae nymph can be distinguished from all of the
are approximately in proportion to the body size, nymphal instars by the presence of a vulva and it
when compared with the adult and the antennal is often very large and distorted from the eggs or
segments are normally, but not always, the same nymphs which she carries in her abdomen. The
in number as in the mature forms. The duration of female nymph has various types of pores on its
the third instar in females is usually about 8 days, body; the circular multilocular and pentagonal
but it can vary under different conditions of tem- quinquelocular pores are believed to function in
perature and humidity. In the male, the second the production of the lamentous ovisac, whereas
skin is shoved to the posterior portion of the the normally more abundant trilocular pores
cocoon; the third-instar male is called the pre- function in the production of the white powdery
pupa and is usually much smaller and more elon- secretion, characteristic of mealybugs. The exact
gated than the third instar female. It also differs function of any of these pores has yet to be con-
because it has wing pads, no rostellum and more rmed and the precise morphological structure of
antennal segments. The duration of the third- the various types of tubular ducts is still unknown.
6 Biology 91

In certain mealybug species, such as Ferrisia vir- these of Pula are very dark brown or almost black
gata, it is believed that the enlarged tubular ducts in colour. Leg size is also quite variable:
produce thin crystalline rods, but the importance Antoninoides have very small, reduced legs;
of the smaller tubular duct remains a mystery. Discococcus have slightly larger legs;
The setae of the cerarii are apparently impor- Phenacoccus, Spilococcus, Chorizococcus and
tant in supporting the laments; again, in most others bear proportionately normal sized legs;
adult female mealybugs, two pairs of dorsal cavi- and the numerous Puto species bear very enlarged
ties or ostioles, as they are called, can be located and robust legs. The adult females of Antonina
submarginally. The posterior pair is on the seventh are totally without legs (apodous); on each sur-
abdominal segment and the anterior pair is appar- face of the posterior part of the trochanter, there
ently on the head. As previously mentioned, the are normally two, sometimes three, small clear
ostioles, when irritated, seem to function in the spots which are sensory in function. On the tarsal
secretion of globules of body uid, perhaps as a segments and on the claw, mealybugs normally
defensive mechanism. It is also believed that these have a pair of spatulate setae, but these are some-
dorsal openings function in the exit of honeydew times absent. The use of these setae is not known,
for consumption by ants. The laments which may but it seems logical to assume that they, in some
be seen so often on the lateral margins of many way, function in clinging to the substrate. The
mealybugs are apparently produced by the clusters vulva, which is always present in the adult
of trilocular pores surrounding the cerarii. female, is the genital opening and functions in
Other structures of the adult female are the copulation and egg laying. In some instances,
antennae, the eyes, mouthparts, legs, spiracles, more than one male is able to mate with a single
vulva, circulus, anal ring, anal lobes, body setae female at one time.
and cerarii. The antennae of mealybugs are li- The anal rings are often of various shapes in
form, with the terminal segments characteristi- different mealybugs, but they all function in waste
cally longer and wider than the preceding ones. elimination. As previously mentioned, these
There is a slight noticeable tapering of the anten- wastes, which are in many instances detrimental
nae from the rst segment to the last and the to the mealybug, are propelled long distances
antennal segmentation varies in number from two from the body by the rapid contraction of the
in some species of Antonina to nine in certain walls of the anal cavity. It is also possible that the
species of Phenacoccus. Antennal shape is anal ring serves as an exit for honeydew intended
important in the eld identication of some sub- for ant consumption and that the long setae of the
terranean mealybugs. The unusually short genic- ring serve as standards to hold the honeydew
ulate antennae of Rhizoecus, Pygmaeococcus and secretion before it is consumed by the ant.
Geococcus are easily recognized, particularly The adult female measures 2.652.80 mm in
when compared with the normal, straight anten- length and 1.751.85 mm in width, and the
nae of most other genera, which makes their eld females are wingless and as they mature, become
identication quite simple. There are often some more sessile. The female mealybug has a soft,
enlarged setae on the apical, two antennal seg- oval and attened segmented body, but the divi-
ments, which apparently act as special sensory sion between the thorax and the abdomen is not
setae. These setae differ from the other antennal distinct.
setae, being larger in diameter and more rounded
at the tip. The eyes of mealybugs are compound
and they function only in distinguishing between 6.1.9 Adult Male
light and dark.
The legs of mealybugs have a characteristic The fth-instar male refers to the adult which is
colour. For example, the legs of Rhizoecus and very complex morphologically and only the easily
Misericoccus are white, those of many species of recognized characteristics are discussed here.
Phenacoccus and Spilococcus are red, while There are two or three known primary types of
92 M. Mani and C. Shivaraju

dermal pores occurring on male pseudococcids. antennae, such as Palmicola palmarum (Ehrhorn).
The rst type is normally clustered in a circular The male has six eyes a ventral pair, a lateral
group on the posterior lateral margin of each side pair and a dorsal pair. The eyes of most males are
of the ninth abdominal segment. In Phenacoccus dark red, with the smaller lateral pair protruding
gossypii Townsend and Cockerell, there is, in more than the other two. The mouthparts of the
addition to the pair of pore clusters on the ninth male are almost nonexistent and are completely
abdominal segment, another pair on the eighth non-functional. All that remains of the mouth is a
segment. These pore groupings apparently form small circular opening found at the posterior mar-
the wax of the long caudal laments. The pores gin of the ventral part of the head. Normally,
which make up these clusters are circular with a there is one pair of wings which develope from
ve-pointed star-shaped lumen, are called stellate the mesothorax; these wings possess two longitu-
pores. Most of the stellate pore clusters also have dinal veins, the anterior one being the radius and
long slender setae, which apparently act as central the posterior one being the media. There is also a
bases for the wax of the caudal laments. It is felt complex of minute basal veins called the costal
that the long anal lobe setae of the females might complex of wing veins. There are three forms of
also function in this manner. The male caudal males, the rst form has fully developed wings
laments of Puto arcloslaphyli Ferris and Puto (macropterous); the second form has wings, but
decorosus McKenzie, herein described as new, they are reduced and nonfunctional (brachypter-
show a seta in the middle of the long waxy la- ous); and the third form is wingless (apterous).
ments. In Phenacoccus gossypii Townsend and Examples of the rst form are Phenacoccus gos-
Cockerell and Pseudococcus longispinus (Targioni sypii Townsend and Cockerell, Planococcus cilri
Tozzetti), the above characteristic was observed in (Risso), Puto lalicribellum Mc- Kenzie
the females. Other types of pores have also been Saccharicoccus sacchari (Cockerell); of the sec-
found on the males and are scattered over the body ond form is Palmicola palmarum (Ehrhorn); and
surface. These are called dermal disc pores and of the third form are Puto ambiguus (Fullaway),
name the number of loculi they contain. These P. echinalus McKenzie and P. pacicus
may vary from three to ve in number with four McKenzie. A pair of halteres is present on the
being normal, and it is further pointed out that metathorax; they are slender projections adorned
these structures are by no means at, but rather are with one or more setae at their tips. The normal
recessed into the derm, with several small protru- number of apical setae is one, but four have been
sions from the central part of the loculi. on each haltere in Puto yuccae (Coquillett). The
Body setae are also characteristic in the male. apical setae, whether four or more in number, are
Just as the normal lanceolate setae of the female re-curved in such a manner so as to hook into a
are present, so also are the thick, nger-like circular pocket in the posterior part of the
digitiform setae described by Beardsley. The lat- forewing.
ter are normally the most common of the two There are two pairs of spiracles in the male,
types; they predominate on both the surfaces of just as in the female, but in the case of the male
the body, the legs and especially the antennae. there is often a much more strongly developed
The digitiform setae, which are presumably peritreme. The legs of most males are quite simi-
sensory in function, are very similar to those on lar to those of the females, although they are usu-
the last two segments of the female mealybugs ally proportionately much longer and more
antenna. slender. The tarsus of the male has two segments
One pair of dorsal ostioles is present on the rather than the normal single segment of the
submarginal portion of the seventh abdominal female, although in most cases the additional
segment and corresponds to the posterior pair of segment is quite small and appears as a slightly
ostioles on the female. The antennae of the adult sclerotized ring. The digitules of the tarsal claws
male normally have ten segments, but occasion- of most males differ from the spatulate type of
ally there are species which have nine-segmented the female in being slender and setiform. The
6 Biology 93

claw is normally without a denticle. The external the young ones are produced over a period of up
genitalia in male is relatively simple, consisting to 2 months. On average, there are 170 offspring
of a large penile sheath, a conspicuous vertical per female during the spring and about 150 in the
slit and the penis or aedeagus. The penile sheath summer. The rst-instar nymphs are motile, but
is normally large and sclerotized with a posterior the succeeding instars are sessile and produce the
apical projection; this projection maybe of vari- felted wax covering from which a characteristic
ous shapes, but is usually broadly oval. On the excretory tube protrudes. A generation may take
ventral surface of the sheath, there is a noticeable 46 weeks, depending upon temperature and
slit from which the aedeagus often protrudes, is location.
normally tube-shaped and curves downward. The
penile sheath is apically of various shapes, from
broad as in Pseudococcus fragilis Brain, to very 6.2.2 Brevennia rehi
sharp and pointed as in P. longispinus (Targioni-
Tozzetti). The male of Puto yuccae (Coquillett), Reproduction of B. rehi Lindinger is mainly by
as well as many others of the Puto group, is quite thelyotokous parthenogenesis, viviparous parthe-
different from the normal Pseudococcid male. nogenesis and, to some extent, by oviparous sex-
The primary differences noted were eight pairs of ual reproduction. The oviposition period has
eyes, four setae on each halter, a toothed and been reported to be 24 days and the total num-
bifurcate aedeagus and a denticle on the claw. ber of eggs laid by a female varies from 42 to
The adult male has a brown-coloured body, 144, although up to 350 eggs has also been
bears two white, anal laments and is about recorded. The eggs are hyaline to yellowish-
1.5 mm in length. The development of the egg to white or pinkish-white and are elongate oval in
an adult male or female mealybug takes about shape. They are laid in groups in between the leaf
2426 days, but this can vary for different species sheath under the mealy covering; the incubation
under different climatic factors in different host period ranges from a few minutes to 39 h, with
plants. The population of the male mealybug is the hatchability of the eggs varying from 41.7 to
generally very low, compared to the females; the 93.5 %. The newly hatched nymphs are crowded
male to female ratio varies from 1:5 to 1:8, but within the waxy threads for 610 h before they
again, this is highly variable for different disperse to various parts of the same plant. The
species. pale yellowish nymph is active and the body gets
The biology of the mealybug varies with dif- covered with the waxy material on the second
ferent temperature conditions. The number of day. The nymphal period varies from 3 to 4
generations is quite variable in the weeks, where the mature females lay eggs for
Pseudococcidae; there are eight life cycles in about the same duration. The male nymphs grad-
approximately 1 year. In most of the Puto spe- ually develop wings after the rst few moults and
cies, however, only one generation occurs annu- emerge as small, active, ying insects; they are
ally and in Puto sandini Washburn, a high-altitude rarely seen and generally mate with females
species, there is one generation every 4 years. before dying a day or two after their emergence.
Adult females are wingless, robust, pink and
6.2 Biology of Important
Mealybug Species
6.2.3 Cataenococcus ensete
6.2.1 Antonina graminis
Ensete root mealybug C. ensete Williams and
The mealybug A. graminis (Maskell) reproduces Matile-Ferrero is a serious pest in southern
unisexually and up to ve generations are pro- Ethiopia. The females are viviparous and pro-
duced each year. Eggs hatch within the body and duce 253 nymphs/females. The average duration
94 M. Mani and C. Shivaraju

of the rst-, second- and third-instar nymphs was non-sexual reproduction occurs. In summer,
16.2, 18.1 and 19.7 days, respectively. The aver- both the species produce living young over a
age lifespan of the adult female is 49.9 days. The 34-week period, with the Dysmicoccus neobre-
body length and width of the adult female mealy- vipes produces 346 offspring per individual and
bugs ranged between 2.94 mm and 2.53.5 mm, D. brevipes produces 246. The rst, second and
respectively, when measured inclusive of the wax third instars or larval stages last for 1026 days,
covering. Adult female mealybugs could not sur- 622 days and 724 days, respectively. Thus, the
vive more than 3 weeks in the soil in the absence total nymphal period varies from 26 to 55 days,
of plant materials. with the average being about 34 days. The pink
form starts reproducing parthenogenetically
about 25 days after the third moult, whereas the
6.2.4 Coccidohystrix insolita gray form produces males in about a 1:1 ratio
and mating is necessary for reproduction.
The adult female has very little dorsal wax and Unmated females may live for nearly 4 months
secretes a white, waxy ovisac up to 6 times as long awaiting fertilization. There are multiple over-
as its own body, which is more typical of some lapping generations, with the life cycle of some
Coccidae. The immature stages do not secrete a being at least twice as long as that of others,
thick layer of mealy wax, the body being shiny reared under similar conditions. Adult females
yellow-green with submedian grey spots on two are plump and have a convex body, and are pink-
abdominal segments and one thoracic segment. ish in colour. Lateral wax laments are usually
The female and male nymphs of C. insolita, less than one fourth as long as the breadth of the
reared in mass on sprouted potato tubers, at 22 body and those towards the back of the insect are
and 33 Cand 6096 % RH, completed ecdysis at half as long as the body. The fecundity of the
the age of 13.92 and 14.60 days, respectively. female was 658.58 nymphs/ovisac and the pre-
The ratio of female:male was 3.24:1. Starvation larviposition period for adult females lasts for
of impregnated females had no adverse effect on about 27 days. The larviposition (giving birth to
their oviposition. The increase in age of impreg- larvae) period lasts for an average of 25 days,
nation from 5 to 40 days in females had little they give birth to about 234 progeny, but may
effect on the preoviposition and oviposition peri- produce up to 1000 crawlers. It may then live for
ods and the incubation period of eggs. Fecundity another 5 days before dying. The duration of the
is about 261 days and the longevity varies from adult female life varies from 31 to 80 days, aver-
17.66 to 51.6 days. Thirty- to forty-day-old aging about 56 days. Male pineapple mealybugs
females showed 7788 % and 9699 % reduction do not exist in Hawaii; they are observed from
in oviposition period and fecundity, respectively. Brazil. Male pineapple mealybug males are dis-
tinguished from the gray pineapple mealybug
males by the difference in the number of anten-
6.2.5 Dysmicoccus spp. nal segments. The pineapple mealybug has eight
antennal segments and the gray pineappple
There are two separate species of Dysmicoccus mealybug has ten. In addition, the pineapple
found on pineapple plants. The pink mealybug mealybug has short clavate setae on its body and
Dysmicoccus brevipes (Cockerell) which repro- appendages instead of the digitiform setae that is
duced non-sexually and the gray mealybug found on gray pineapple mealybugs. The dura-
Dysmicoccus neobrevipes Beardsley which was tion of the adult female life varies from 31 to 80
bisexual. D. brevipes reproduces non-sexually days, averaging about 56 days, where, the pre-
through a process called parthenogenesis in larviposition, larviposition and post-larviposi-
which females birth female larvae without fertil- tion periods last for an average of 27, 25 and 5
ization by males in Hawaii. In areas such as days, respectively. They give birth to about 234
Brazil, where males are present, both sexual and progeny, but may produce up to 1000 crawlers.
6 Biology 95

Another species Dysmicoccus boninensis yellow) remain motionless for 1015 min before
(Kuawana) is oviparous. The eggs are laid in a moving to the tender parts of the plant to x them-
cottony ovisac and hatch in about 10 days. The selves for feeding. The average duration of the rst
nymphal period ranges from 18 to 26 days and instar is 6.7 days and it takes about 4.4 days from
the males are necessary for reproduction. rst moult to cocoon formation in MarchApril. In
Dysmicoccus carens Williams was viviparous the cocoon, males moult three times and their
with four nymphal instars preceding the adult development inside the cocoon takes about 9 days.
stage. The life cycle of the mealybug ranges from The total nymphal period is about 20 days in
48.2 to 63.8 days when reared on CoC 671 or Co males. Thus, an adult male emerges from the
740. The mean fecundity is the lowest (117.6 cocoon after the fourth moult and is ready for cop-
crawlers/adult female) when reared on Co 6907 ulation a little after emergence. The male adults
and the highest (230.6 crawlers/adult female) on live for 13 days. Females undergo three nymphal
C 740. The longevity of males is 34 days. The instars and pass through incomplete metamorpho-
longevity of females is the greatest (32.3 days) on sis. The duration of the rst, second and third
Co 740 and the shortest (18.0 days) on CoC 671. instar was 7, 6 and 6 days, respectively. Total dura-
The mean duration of the rst instar varies from tion of the nymphal stage in females averages
4.8 days on CoC 671 to 6.1 days on Co 6806. The between 43.2 and 92.6 days at 28.9 and
duration of the second instar is the shortest 16.6 deg C, respectively, while in males it aver-
(4.1 days) on CoC 671 and the longest (5.8 days) ages to 25.4 days at 26.5 C. The total lifespan,
on Co 7704. The duration of the third instar was from the egg stage to the end of the adult stage,
the shortest (5.1 days) on CoC 671 and the lon- averages about 76.2154.6 days in females as
gest (6.1 days) on Co 6806. The duration of the opposed to 1947 days in males. The male:female
fourth instar ranged from 13.5 days on Co 6907 sex ratio is 1:1.87. Adult females are apterous with
to 15 days on Co 7704. two long prominent waxy laments at the poste-
rior end and with a lot of waxy or glossy hair over
the body which is covered with white waxy pow-
6.2.6 Ferrisia virgata der. They have fairly long, dark stripes on the dor-
sum of the posterior end of the body.
Reproduction in F. virgata (CklI.) is by both sex-
ual and parthenogenetic means, but the latter is
more common in this species. The courtship lasts 6.2.7 Ferrisicoccus psidii
for 130 min and the copulation time ranges from
15 to 20 min. The males prefer young adult In F. psidii Mukhopadhyay and Ghose, the duration
females and mating occurs only once during the of the rst nymphal stage ranges from 4 to 11 days.
lifespan of the female. The longevity of the female The second- and third-instar female nymphs com-
is about 50 days and the fecundity ranges from 300 plete their moulting at the age of 15.5 and
to 700 eggs per female. The eggs are deposited in 21.35 days, being 66.8 and 60.0 % at the age of
groups, rarely singly and are usually concealed 1317 and 1922 days, respectively. In he second,
under the body. They are oval and buff to light yel- third and fourth instars, males moult at the age of
low in colour. Since the eggs are laid in an 13.28, 14.71 and 18.69 days and are around 69.4,
advanced stage of embryonic development, they 62.4 and 68.5 % developed at the age of 1114,
hatch soon after the oviposition in a very short 1316 and 1720 days, respectively. The colour of
time and are therefore seldom seen. Under normal the crawlers and all the nymphal instars of females
conditions, the egg hatching percentage is about are rosy, creamy pink, pinkish chocolate and choc-
95 %. The egg period lasts about 28.14 min. Pre- olate; waxy dusts are found on their dorsum, the
oviposition, oviposition and post-oviposition peri- quantity progressively increasing with the progress
ods are 6.4, 8.1 and 1.5 days, respectively. Upon of their development and the stage. Nymphal
hatching, the crawlers (0.34 mm long and light instars of females secrete 78 pairs and 13 pairs of
96 M. Mani and C. Shivaraju

marginally waxy tassels, mostly abdominal. All the ized by well-developed wing pads and lasts for
instars of females and the second instar of males about 57 days. The duration of development,
secrete a tubular and waxy anal process. from egg to adult in case of the female and the
male, is 30.3 and 28.7 days, respectively. The
pre-ovipositional period ranges from 6 to 7 days
6.2.8 Kiritshenkella sacchari and the ovipositional period ranges from 7 to 9
days, while the fecundity ranges from 426 to 573
The eggs of K. Sacchari (Green) are laid in a eggs. Adult males are orange coloured, minute
chain containing nearly 120 smooth eggs beneath and very active. The longevity of adult females
the abdomen of the female. The incubation period range between 13 and 16 days and for males
is 14 h when the average temperature is 27.8 C between 3 and 5 days.
and humidity is 63 %. Freshly emerged nymphs
remain beneath the abdomen of the mother for a
short while, after which they turn restive and 6.2.10 Nipaecoccus viridis
move about to settle in the vicinity of the mother.
The total life cycle is completed in 18.6 days dur- Adult females of N. viridis (Newstead) are rather
ing April. large and have black or purplish bodies. They
appear to be at, having short laments around
the margin, whereas the males are winged with
6.2.9 Maconellicoccus hirsutus long antennae. The eggs are laid in clusters and
enclosed in a protective, cottony mass. A female
Parthenogenesis was the main mode of reproduc- lays about 300500 eggs in its life time; the eggs
tion in M. hirsutus (Green), but sexual reproduc- are purple in colour and hatch in 1020 days and
tion was also observed. Freshly laid eggs are soon envelope themselves in the uffy material.
translucent and yellowish or light orange in The nymphs are amber coloured with whitish,
colour. They are elongated and oval in shape. As waxy coating around the margins. Female nymphs
the incubation period advances, the translucent moult thrice and complete their life cycle in 68
eggs become pinkish in colour before hatching. weeks, while the males moult four times and after
The incubation period varies from 5 to 7 days; passing through a pre-pupal stage, emerge as
and the hatching percentage of the eggs is about winged adults. The average developmental peri-
90 %. The rst-instar nymphs are usually yellow ods of males and females are 18.19 and 16.19 days,
to orange in colour with reddish compound eyes. respectively. The average pre-oviposition, ovipo-
The neonate larvae are oval in shape and are sition and fecundity are 7.33 days, 8.33 days and
highly mobile; during this stage, males and 176.33 eggs, respectively.
females are indistinguishable. The duration of the
rst-instar nymph lasts for 79 days. The body is
pinkish in colour with white, thin and waxy 6.2.11 Paracoccus marginatus
secretions on the body. The duration of the
second-instar nymph lasts for 68 days; at the A single female of Pa. marginatus Williams and
end of second instar, the female nymphs moult as Granara de Willink is known to lay about 230
usual, like the previous instars, but the males 400 eggs in an ovisac. The ovisac, developed
secrete a cottony puparia around their body. The ventrally, is three to four times the length of the
duration of the last instar of the female nymph body and is entirely covered with white wax. Egg
lasts for 810 days. The third-instar male nymphs laying usually occurs over a period of 12 weeks.
are recognized by denuding the puparia, distin- The eggs are greenish-yellow and egg hatching
guished by the presence of two small wing buds. occurs in about 10 days. The males have four
This instar lasts for 12 days, with an average of instars; the rst-instar nymphs are called crawlers
1.4 days. The last instar male nymph is character- and the duration of the rst-, second-, third- and
6 Biology 97

fourth- instar in the male nymph at 25 C was 6.5, 9.08 days, 67.42 eggs per female and 4.57 days,
6.6, 2.4 and 41 days, respectively. The fourth respectively. The longevity of the adult females
instar is produced in a cocoon and is referred to range from 47 to 55 days and the species repro-
as the pupa. Adult males tend to be pink in colour, duces parthenogenetically.
especially during the pre-pupal and pupal stages,
but appear yellow in the rst and second instar.
The duration of the rst-, second- and third- 6.2.14 Phenacoccus herreni
instar of the female nymph in the mealybug was
6.5, 5.5 and 5.2 days, respectively at 25 C. The Phenacoccus herreni Cox and Williams is a sex-
species is known to reproduce both sexually and ually reproducing mealybug. The rst instar
parthenogenetically. Males have longer develop- nymphs (crawlers) complete their development
ment time (2730 days) than females (2426 in an average of 7.7 days, the second instar aver-
days). The mean longevity of adult males and ages to 5.1 days and the third averages to 5.6 days.
females was 2.3 and 21.2 days respectively. The Adult females live for an average of 24.8 days,
adult female body is greenish-yellow, dusted with the oviposition period averaging about
with mealywax and not thick enough to hide the 18.4 days. The males passed through two
body colour without discrete bare areas on the nymphal instars, a pre-pupal stage and a pupal
dorsum and with many short waxy laments stage before becoming adults; these average at
around the margin of the body. around 7.5, 6, 2.8 and 3.1 days, respectively. The
ratio of females:males was 3:1. Reproduction
was exclusively sexual; oviposition begins 3 days
6.2.12 Phenacoccus aceris after pairing and the females deposit an average
of 773.6 eggs each. Initially, the crawlers are
Female Ph. aceris Signoret starts laying 200500 found mainly on the growing point of the plant,
eggs in a cottony ovisac during a 2-week period. from which they disperse down the stalk, settling
The eggs are oval and lemon-yellow in colour. nally on the lower surface of the leaves.
The ovisacs contain up to several hundred eggs.
The rst instar nymph is lemon-yellow, but with
bright red eyes. The nymphs gradually disperse 6.2.15 Phenacoccus madeirensis
to nearby plant tissues. Soon after they begin
feeding, they develop a granular white waxy cov- The total duration of development of the female
ering with laments at the caudal end, which is Phenacoccus madeirensis Green is 30 days at
typical of mealybugs. The adult female has a sage 25 C, 46 days at 20 C and 66 days at 15 C. The
green body, which is visible through the white, developmental time of males was 39 days lon-
waxy coating. The tails on the caudal end of the ger than females. Adult longevity at 25 C for
mealybug are shorter and the colour of the body males and ovipositing females was 3 and 20 days,
ranges from greenish to pale purple. respectively. Females at 20 C produced the high-
est number of eggs (500 eggs/female).

6.2.13 Phenacoccus bengalensis

6.2.16 Phenacoccus manihoti
At 28.832 C and 8896 % RH, the nymphs of
P. bengalensis Pramanik and Ghose complete In the case of Ph. manihoti Matile-Ferrero, no
their ecdysis at the age of 20.01 days and all of males are observed and reproduction is by thely-
them become adult females. The females start tokous parthenogenetic means. The eggs are
oviposition at the age of 3142 days. The pre- enclosed in an ovisac of felted waxen threads and
oviposition and oviposition period, fecundity and about 700 eggs are laid by one female. The adult
incubation period of eggs are 14.20 days, females mean longevity is 34.3 days. The dura-
98 M. Mani and C. Shivaraju

tion of the egg stage, rst instar (crawler), sec- produces a sac with a cottony covering protrud-
ondfourth instars and the adult stage averages ing from the anal end of the body. The incuba-
about 8.0, 4.5, 4.1, 4.2, 5.2 and 20.2 days, respec- tion period of the eggs is 6.6 days; the female
tively. The mean generation time is 28.48 days. nymphs moult three times, while the males
moult four times. The freshly emerged rst
instar nymphs are oblong in shape. The average
6.2.17 Phenacoccus peruvianus duration of the rst-, second- and third-instar
nymphs is 4.8, 5.6 and 6.4 days, respectively,
Adult females are elongate oval in shape, are with the total nymphal duration being 16.8 days
greyish with a green tinge and covered in a thin in females. The rst- and second-instar nymphs
layer of white mealy wax. They lack marginal are pale yellow in colour and oblong-shaped.
and caudal wax laments, which are well devel- During the third instar, a white waxy substance
oped in other mealybug species. No males are covers the dorsal body surface. The adult
observed in the case of Ph. peruvianus Granara female is oblong in shape, light to dark yellow
de Willink and they reproduce parthenogeneti- in appearance and is wingless. The pre-
cally. Eggs are laid in the highly conspicuous oviposition, oviposition and post-oviposition
white, waxy and elongate ovisacs that form dense periods are recorded as 4.3, 8.0 and 2.7 days,
groups on the undersides of the foliage and on the respectively. The female adult survives for
stems. The nymphal instars are pale orange in 15.5 days and the entire lifespan lasts about 31
colour. days. A pair of dark spots on the thorax and
three pairs on the abdomen forming two longi-
tudinal stripes are noticed. Male mealybugs
6.2.18 Phenacoccus saccharifolii have two nymphal instars. The mean duration
of the rst and second instar is 4.0 and 5.3 days,
The female Ph. saccharifolii Williams secretes respectively. At the end of the second nymphal
the ovisac probably from the accessory glands instar, the males construct the puparia. The
one or two days prior to oviposition. The gravid pupal duration ranges from 6 to 7 days. The
female lays about 700 eggs in a single ovisac in total development of the female is complete in
batches. By the time the last batch of eggs is laid, about 26 days, while that of male takes about
the body of the female is raised to a vertical posi- 18.33 days. The sex ratio is 1:1.29.
tion with the anterior end attached to the substra-
tum by the oral bristles. The female dies soon
after oviposition. The incubation period lasts for 6.2.20 Planococcoides njalensis
56 days. The total life cycle is completed in
2528 days. This mealybug, Pl. njalensis (Laing) is biolog-
ically variable. Some of the forms exhibit a
strong parthenogenetic habit, so that males are
6.2.19 Phenacoccus solenopsis not necessary, whereas the others require males
for reproduction. Fecundity is very low, aver-
Phenacoccus solenopsis (Tinsley) is observed aging only about 36 young ones per female
to be ovoviviparous; the adult female is capable over a 20-day adult lifespan. The eggs hatch
of reproducing only if she mates with a male. P. within a few moments of being laid. There is
solenopsis lays about 500 eggs in the ovisac; no ovisac, only a few thin laments being pro-
they are minute, oval in shape and light yellow vided by the female for temporary protection
in colour. The eggs are smooth, translucent of the young. The life cycle is completed in
oblong in shape with tapering ends. It retains its about 42 days and there are about eight genera-
eggs in the body until they are ready to hatch. It tions in a year.
6 Biology 99

6.2.21 Planococcus citri Coccidoxenoides perminutus Girault at ve tem-

peratures between 18 and 30 C. The intrinsic
The female Pl. citri (Risso) lays yellowish-white rates of increase (rm) for both species were simi-
eggs within the ovisac. There may be 300800 lar, reaching maxima at 25 C (rm = 0.169 for P.
eggs in one mass and the eggs are oval and glossy. cus; rm = 0.149 for C. perminutus). The net
They hatch within 610 days; the nymphs are replacement rate (Ro) of P. cus was higher than
yellow, oval-shaped with red eyes and covered that of C. perminutus at all ve temperatures
with white waxy particles. The female nymphs tested. The Ro of P. cus reached a maximum at
have four instars, while the males have three 21 C (308.87 days) and that of C. perminutus at
instars and a pre-pupal stage. Only the males can 25 C (69.94 days). The lower and upper thresh-
produce a cottony cocoon and pupate. The male old temperatures for development of P. cus are
nymphs are elongated and narrower in appear- estimated at 16.59 and 35.61 C, respectively.
ance than females and often occur in a loose The lower threshold for the development of C.
cocoon. A female nymph is full grown in 68 perminutus was 8.85 C, but the upper threshold
weeks with three moults. The male is winged, could not be determined as there was no turning
greyish in colour and midge-like with long anten- point on the graph. Both the insects were well
nae. The male nymphs spin cotton-like cocoons, adapted to the temperatures. An average of 360
23 weeks after hatching and pupate before eggs per female was recorded.
transforming themselves into winged adults with
four moults, completing many overlapping gen-
erations in a year. The total life cycle of this 6.2.23 Planococcus kenyae
mealybug is completed in 3035 days. Citrus
mealybug populations are generally composed of An adult female of P. kenyae (LePelley) produces
equal numbers of males and females. The females more 150 progeny. The eggs are laid in a small,
are wingless, white to light brown in colour, with light ovisac and hatch in about 1.5 days, but this
brown legs and antennae. The body of adult period varies with climatic conditions from 1 h to
females is coated with white wax and bears a 45 days. The development from the egg to the
characteristic faint gray stripe along the dorsal adult stage requires about 36 days for the female
side. Short waxy laments can be seen around the and 33 days for the male.
margins of their oval body, with a slightly longer
pair of laments present at the rear end. The
females live for up to 29 days, depending on the 6.2.24 Planococcus krunhiae
host plant. The males are similar in colour to
females and have two long backward-projecting In the case of Planococcus krunhiae Kuwana, the
white wax threads. The adult males are winged duration of development from the egg to the adult
and thus capable of ying to new host plants for stage takes 35 days at 28.7 C and 80 % RH. The
the purpose of mating. Following their emer- duration of the egg and the nymphal stage is 4
gence, males live for 12 days, during which they and 20 days, respectively. Female lays about 150
are incapable of feeding. The males are short- eggs per female. Male mealybug takes 25 days to
lived, ranging from 2 to 4 days after the nal complete life cycle. Egg hatchability is about
nymphal moult. The females, however, live for 95 %.
3040 days.

6.2.25 Planococcus minor

6.2.22 Planococcus cus
The eggs of passionvine mealybug Pl. minor
Life table analyses were conducted for (Maskell) are yellow, minute and are protected in
Planococcus cus (Signoret) and its parasitoid an ovisac. At 29 C, the eggs hatch in 5.7 days.
100 M. Mani and C. Shivaraju

The duration of the rst and second instar(female), called a pre-pupa, is contained in a cocoon that
the second instar (male), the third instar(female), begins forming toward the end of the second
the third instar (m) and the fourth instar(M) are instar. The fourth stage of the immature male is
6.6, 7.2, 6.4, 6.9, 2.6, 5.9 days, respectively. The the pupa; it is elongated and light reddish-brown.
females take 30.8 and males take 27.5 days, At 30 C, a generation may be produced in 2729
respectively, to complete the development cycle. days.
Fecundity is about 180 eggs and the male:female Adult females and males emerge at the same
ratio ranges from 1:1.54 to 1:2.75. time, from late June to mid-July for the rst
(overwintering) generation and late August to
mid-September for the second (summer) genera-
6.2.26 Pseudococcus comstocki tion. Adult females are present for a total of 46
weeks and oviposit for about 1 week after mat-
Pseudococcus comstocki (Kuwana) is known as a ing. The males survive for only a few days after
pest of pome and stone fruits and certain orna- emerging. The overwintered eggs hatch from
mental plants. There are two, three, or even four mid-April through May and the nymphs (crawl-
generations per year, depending to some extent ers) migrate from the oviposition sites to their
on climate. Generally, there is little overlapping feeding sites on terminal growth and to the under-
of broods until late in the season. Overwintering sides of the leaves of trees and shrubs. This hatch
is in the egg stage within the cottony ovisac. is completed by the petal-fall stage of pears. The
Overwintering eggs are laid as early as October, nymphs that hatch from these overwintered eggs
even in the milder climates, such as that of cen- are active from roughly early May to early July.
tral California. The overwintering eggs generally As the nymphs approach the adult stage, they
start hatching in late spring; they are elliptical tend to congregate on older branches at a pruning
and bright orange-yellow in colour. They are laid scar, a node, or at a branch base, as well as inside
in jumbled masses along with the waxy lamen- the calyx of pears. The second (summer) genera-
tous secretions in protected places such as under- tion nymphs are present from about mid-July to
bark crevices, near pruning cuts and occasionally mid-September.
in the calyx of fruits. The summer-generation
eggs are laid from mid-June through late July and
the overwintering ones from mid-August to 6.2.27 Pseudococcus cryptus
October. The summer-generation eggs have an
incubation period of about 11 days; the females Egg development time in Ps. cryptus (Ps.citricu-
produce an average of 200300 eggs, although lus) Hempel decreases with increasing tempera-
some individuals produce up to 700. The young ture and ranges from 2.4 days at 16 C to 1.0 days
females develop through three instars, after at 28 C. The total development time of nymphs
which they are capable of being fertilized and decreases from 54.9 days at 16 C to 17.4 days at
oviposition follows after 1015 days. The rst- 28 C and 19.3 days at 32 C. P. cryptus shows an
and second-larval instars of the female and the ovoviviparous reproductive behaviour and hence
male mealybug are virtually indistinguishable. the egg period is combined with the rst-instar
They appear similar to adult females, except that nymph. By tting linear models to the data, the
they are smaller, more oval-shaped, lack the long lower developmental threshold temperatures for
body laments and are more orange-yellowish the egg to the rst nymphs, second nymphs, third
because they have a lesser amount of wax cover- nymphs and from the egg to the third nymphs are
ing them. The rst-instar female crawler is at calculated as 8.7, 12.8, 13.1 and 12.1 C, respec-
and pale yellow but become darker over time. tively. The thermal constants are 198.6, 84.7,
The second and third instar females are similar in 69.8 and 296.3 degree-days, respectively, for
appearance, but become progressively browner each of the above stages. The non-linear model
and redder. The third instar of the immature male, based on a Gaussian equation, used to predict the
6 Biology 101

relationship between development rate and tem- similar to that of the other mealybugs. At the end
perature, is well described for all the stages. In of the second instar, the males produce cocoons
addition, the adult longevity decreases from (pupa) over their bodies. The third moulting takes
80.4 days at 16 C to 31.3 days at place within the cocoon; the fourth instar, also
32.0 C. Furthermore, the pre-oviposition and known as pupa, is characterized by well-devel-
oviposition periods show a pattern similar to that oped wing pads. Only males pupate and develop
of longevity. Overall, P. cryptus has a maximum into adult males. The male development, includ-
fecundity of 111 eggs per female at 28 C, which ing the nymphal and pupal stages, ranges from 18
declines to 102.7 eggs per female at 32 C. to 20 days with a mean of 19.10 days. The adult
female mealybugs are very sluggish and are simi-
lar to the nymphs. The male mealybugs are rare,
6.2.28 Pseudococcus jackbeardsleyi tiny and active. They have a pair of wings and two
long waxy caudal laments at the posterior end of
The Jack Beardley mealybug Ps. jackbeardsleyi the abdomen, similar to the other mealybugs.
Gimpel and Miller is oviparous and lays yellow- They are y-like insects, do not feed and die soon
ish eggs. The eggs are laid in a mass within a after they mate. The females complete the life
loose, thin and waxy sac behind their abdomen. cycle in 2529 days, with a mean of 26.20 days
The ovisac is a little elongated and the number of and while the males complete their development
eggs laid by a single mealybug ranges from 650 to in 2326 days, with a mean of 24.40 days. There
900 with a mean of 775.60. They are in close is a variation in the developmental period from
proximity within the white ovisac. Freshly laid eggs to adults in the mealybugs, depending on the
eggs were yellowish, smooth and oval with weather and host plants.
slightly tapering ends, but they turn a darkish yel-
low before they hatch. The incubation period is
58 days, with a mean of 5.37 days at 25 1.8 C 6.2.29 Pseudococcus longispinus
and 7085 % RH. The nymphs remain in the egg
sac for a day or two after hatching, before crawl- The female Ps. longispinus (Targioni-Tozzetti)
ing about the plant in search of food. Newly produces around 200 live young (which she
hatched mealybugs (crawlers) are quite active. deposits under her body) over a 23-week period.
The crawlers, once they begin feeding, secrete a During summer, the life cycle is completed in
white, waxy material that covers their body and around 6 weeks and in about 12 weeks in winter.
produces approximately 34 leg-like laments Long-tailed mealybugs produce live young, but
around the perimeter of the body. The nymphs are do not produce an ovisac. The eggs are straw yel-
light yellow and six-legged with oval, attened low at rst, but deepen in colour before hatching.
and smooth bodies. The females change only The eggs (20240) may hatch as soon as they are
slightly in appearance, except for growing in size laid, giving the impression that the young are
to about one sixth or one fourth of an inch when born, rather than hatched. The crawlers are at,
fully grown. The females of this species have oval, light yellow in colour and six-legged insects
three larval stages (or instars); similar to the other with smooth bodies. Soon after beginning to
mealybugs, the male and female nymphs are feed, they exude a white, waxy covering over
indistinguishable in the rst instar, but by the end their bodies. The differentiation between the
of the second instar, it is possible to differentiate male and the female begins only after moulting.
between the sexes. Female mealybug nymphs are The male nymphs stop feeding near the end of the
similar to that of adult female mealybugs, except second stage and migrate towards a protected
the latter are larger in size. The females become place where they secrete waxy cocoons in which
adults after the last moult; the female nymphal they complete their development. The females go
period ranges from 18 to 21 days with a mean of through three stages to adulthood, but change
20.82 days. The males have four nymphal instars, little in appearance.
102 M. Mani and C. Shivaraju

6.2.30 Pseudococcus mandio has ve. The pre-oviposition period is 12 days and
the eggs laid by the gravid females are observed on
At 25 C, 80 % RH and constant light, the female the underside of their abdomens. Fecundity ranges
Ps. mandio Williams has three nymphal instars, from 200 to 300 eggs per female; they are creamy
with average durations of 9.2, 5.7 and 6.5 days, yellow and covered with mealy powder. The rst-
respectively and their average lifespan is 17.8 days. instar nymph is cream-coloured and after the rst
The males have two instars, which last an average moult, the cream-yellow colour changes to light
of 8.9 and 5.2 days, with the average pre-pupal and pink. The nymphs feed together for some time and
pupal periods of 12.5 days, and an average adult a few days before the second moult, the nymphs
lifespan of 2.1 days. The pre-oviposition period developing as males spin a cocoon. Such male
lasts 4.7 days and each female lays an average of nymphs descend from the stalk of young plants and
302.2 eggs. The average incubation period is pupate in the leaf sheaths, while the female nymphs
3.8 days, with 99.4 % eclosion. The life cycle from remain feeding on the leaves. This stage lasts for
oviposition to adult emergence is 25.2 days for 67 days. The pre-pupa appears pink in colour and
females and 30.4 days for males. lasts for 2 days. In the case of males, the pupa is
distinguished from the pre-pupa by the presence of
wing pads. The pupa moults once again to attain the
6.2.31 Pseudococcus maritimus adult form; the adult male is a small, delicate and
alate insect with a reddish-pink body. The lifespan
Both sexes of Ps. maritimus (Ehrhorn) are capable of the male is only days. In the case of females, the
of mating multiple times on the same day and on light pink second-instar nymph is covered by mealy
sequential days. Median times between copula- secretion and this stage lasts for 6 days. Third instar
tions are short (<10 min) on the rst day that the nymph is light pink and covered with copious secre-
males are presented with the females, but tend to tions of wax. The yellowish-brown adult female is
increase with sequential copulation events. densely covered with wax, very sluggish and sel-
Unmated females live for up to 19 weeks, as mat- dom moves away from the spot of feeding. The
ing and oviposition result in reduced longevity. lifespan of the adult female, including the pre and
The eggs that are laid are yellow to orange in post-gestational period, is 2527 days.
colour and are within an egg sac. The crawlers are
yellow to orange-brown in colour. There is a stron-
ger winter dormancy in the egg and crawler stages, 6.2.33 Pseudococcus viburni
so that the seasonal development is attuned to a
deciduous host. Overwintering usually takes Pseudococcus viburni (Signoret) (=Pseudococcus
places ordinarily in crawlers and unhatched eggs obscurus Essig; Ps. afnis (Maskell)) has four or
in the loose cottony ovisac. With the rst warm ve generations per year on citrus, depending on
weather of early spring, these nymphs move to the the climate. It overwinters in all stages, with mod-
swelling buds and feed on the tender shoots; on erate retardation from cold weather. Each female
reaching maturity, they begin to oviposition around deposits up to 500 eggs during the rst 12 weeks,
June or July. The mature females tend to move to which accumulate in a loose caudal egg sac. They
the trunks or protected crevices of the rough bark hatch in about 8 days under summer conditions
to oviposition. It is this brood which, by feeding on and maturity is attained in about 42 days, fol-
the leaves and the fruits, causes the damage. lowed by oviposition after several weeks.

6.2.32 Pseudococcus saccharicola 6.2.34 Rastrococus iceryoides

Parthenogenesis and sexual reproduction are the The female R. iceryoides Green lays eggs only
common modes of reproduction in this species. after fertilization. The pre-oviposition period
While the female undergoes four instars, the male lasts for 79 days and the oviposition lasts for
6 Biology 103

7 days. About 500 eggs are laid in the white may be found swarming from below the mother,
ovisac and the fecundity averages to about 800 which tend to give an impression that the mealy-
eggs. The incubation period is 6 days. Females bug is viviparous. The crawler extricates itself
moult three times, while males moult four from one end of the egg, the eggshell sticking on
times to become adults. The females take its posterior end. The rst-instar nymphs are tiny,
2030 days and males 1825 days to complete transparent and pink in colour and very active.
the life cycle. This stage lasts for 5.3 days. During the second-
instar nymphal period, the body grows in size and
the antennal length increases to 0.36 mm due to
6.2.35 Rastrococcus invadens the addition of a segment. The stage is completed
in 4.83 days. The duration of the third-instar
The mealybug, R. invadens Williams completes nymph is 17.2 days. Ovarian development is
eight generations in a year. The female and completed in 13.8 days while one generation is
male nymphs complete development in 34.67 completed in 54.7 days.
and 38.16 days, respectively, during winter at
1521 C and in 24.6332.67 days or 27.63
36.18 days at 1833 C during February to 6.2.37 Trionymus haancheni
November, the optimum being during June
July at 2731 C in females and during May The adult female Trionymus haancheni McKenzie
June at 2733 C in males. The male:female is quite small, but is visible to the eye without
ratio ranges from 2.13:1 to 3.3:1. The maxi- magnication, reaching a length of approxi-
mum pre-reproductive period and oviposition mately one fth of an inch (5 mm). The eggs are
period and minimum fecundity are 2029 days, laid in loose, cottony wax. These cottony egg
3445 days and 165 (145175) in nymphs, sacs are usually laid on the lower part of the
respectively, in winter. The minimum pre- plant, close to the roots and were also observed
reproductive period and the maximum fecun- under the leaf sheaths of the plant. A single
dity are 1418 days and 204 (180235) days in female can lay as many as 256 eggs in a single
nymphs, respectively, in September and the ovisac during a week. Reproduction occurs asex-
minimum oviposition period (2835 days) ually in the absence of males. The eggs are pink-
occurs in April. red and not visible to the naked eye. Eggs hatch
producing the crawlers (the most mobile nymphal
stage, which disperse to nd suitable sites for
6.2.36 Saccharicoccus sacchari feeding on plant sap). The crawlers can also be
transported to other plants by wind, people, or
In the largely parthenogenetic mode of reproduc- animals; they develop through several successive
tion, alate males are not uncommon, though nymphal instars that resemble small adults, each
apterous forms are also observed in the case of of which have legs and can actively move, until
Sa. sacchari (Cockerell). With a pre-oviposition the mature adult stage is reached and the cycle
period of 13.83 days, a single female is capable repeats. The number of generations in Idaho is
of depositing nearly 1,000 eggs. The eggs are still unknown but all the instars can be found at a
smooth, yellowish, cylindrical, with both ends single time on a plant host. The number of gen-
rounded. A single such batch may contain a max- erations is not known, but all the stages have been
imum of 262 eggs. The nymphs hatch within found co-existing on infested plants. Coupled
34.15 h and before hatching, the eggs become with a short generation time, the ability to repro-
soft and elongated. Sometimes, no eggs may be duce asexually can allow mealybug infestations
noticed and only orange coloured tiny crawlers to increase quickly to damaging levels.
104 M. Mani and C. Shivaraju

6.3 Biology of Root Mealybugs 6.3.2 Paraputo sp.

6.3.1 Geococcus citrinus Kuwana They are bisexual and can be ovoviviparous or
viviparous. The favourable period for their repro-
This is a bisexual species. The females lay the duction is around AugustOctober, with 30 nymphs
eggs in masses or chains. These eggs are pearly per female mealybug. The nymphs develop into
white, translucent and elongate oval in shape. both male and female adults. The males are charac-
The average incubation period is 12.20 days. In terized by one pair of wings, are shorter in size than
Gococcus citrinus, a single female is known to the females and occur in very few numbers. The
lay about 113188 eggs, with an average of females are plump, convex in shape and covered
128.2 eggs. There are three nymphal instars for with white waxy mealy substances. They develop
the females; the nymphs are elongate oval, white by undergoing three nymphal instars, while the
in colour and cluster on the roots to feed. The males undergo four growth stages. The life cycle of
duration of the rst-, second- and third-instar the females takes 33.543.7 days, while that of the
nymphs lasts for an average of 7.3, 5.6 and males take 29.339.5 days.
5.8 days, respectively. The size of the nymphs
increases with the instars. In males, the pupal
stage lasts for 5 days. The adult females are 6.3.3 Cataenococcus ensete
elongate oval, white and wingless with a seg-
mented body. The females live for about Adults of enset root mealybug C. ensete (Williams
12.78 days. The adult males are light brown in and Matile-Ferrero) are viviparous and produce
colour and have only one pair of narrow, elon- 156383 nymphs, and their total lifespan is 94113
gated and opaque wings with a round outer mar- days. This species has three nymphal stages; the
gin. The males live for a maximum of 5 days. development of the nymph to the adult mealybug
Unlike other mealybugs, G.citrinus nymphs and takes 54 days on average and the lifespan of the
adults do not produce honeydew; hence usually adult root mealybug is 50 days. The average dura-
these are not associated with ants. The total life tion of the rst-, second- and third-instar nymphs
cycle of G. citrinus and Geococcus coffeae is 16.2, 18 and 20 days, respectively. The average
Green are 28.8 days and 33.8 days, respectively. lifespan of the adult female is 50 days.
In case of Rhizoecus hibisci Kawai and
Takagi, the eggs are laid in white, loose, waxy,
elongate ovisacs which are about 2 mm long and 6.3.4 Rhizoecus amorphophalli
can easily disintegrate when disturbed. Each ovi-
sac contains up to 80 eggs, which usually hatch Rhizoecus amorphophalli is the noxious pest
within 24 h. Nymphs (immature stages) are infesting the stored tubers of elephant foot yam,
creamy-white. They closely resemble the adults, taro and tannia. The ovoid, pale white eggs are laid
but are signicantly smaller. Adult females are in clusters inside the egg sac and turn light brown
creamy-white, elongate and covered in a pow- on hatching. The average length and breadth of the
dery wax that is deposited on the roots and the eggs are 187.80 m and 102.50 m, respectively.
soil; these deposits are often the rst sign of After eclosion, the rst-instar larvae (crawlers)
infestation. Adults and nymphs feed on the roots moved out of their ovisac, actively searching for
of the host plants, but may also be found within suitable feeding sites on the tubers. The crawlers
the root ball and on the inner surface of the plant are oval and semi-translucent with three pairs of
container. The males are extremely rare and are legs and paired eyes, measuring 183 m in length
unlikely to be seen. There can be several over- and 98 m in width. They prefer to hide out in the
lapping generations throughout the year and crevices or depressions of the tubers and on settle-
their numbers can multiply rapidly under favour- ment produce mealy substance to create waxy
able conditions. laments over their body. The rst instar lasts for
6 Biology 105

47 days. The second-instar larva is 270 m long Bartlett BB (1978) Pseudococcidae. In: Clausen CP (ed)
Introduced parasites and predators of arthropod pests
and 124.74 m wide and is semi-translucent with
and weeds: a world review. USDA-ARS, Washington,
a shiny body. The second-instar larva lasts for an DC, pp 137170
average of 4.82 days and before undergoing next Chong JH, van Iersel MW, Oetting RD (2004) Effects of
moulting, they settle either on the previous site or elevated carbon dioxide levels and temperature on the
life history of the Madeira mealybug (Hemiptera:
on another suitable site on the tuber and cover
Pseudococcidae). J Entomol Sci 39:387397
themselves with mealy laments. The third instar Coumara Radja N (1985) Studies on the biology and con-
is relatively larger, measuring 429.47 m in length, trol of rice mealybug, Brevennia rehi (Lindinger)
193.2 m in width, and the duration of this instar (Pseudococcidae: Hemiptera). MSc thesis, Tamil
Nadu Agricultural University, Coimbatore
is 46 days and the sex differentiation is obvious at
Daane KM, Rodrigo PP, Almeida, Bell VA, Walker JTS,
the end of this stage. The female nymphs moult Botton M, Fallahzadesh M, Mani M, Miano JL, Sforza
normally, but the male instar produces a cottony R, Walton VM, Zaveizo T (2012) Biology and man-
puparium around its body.. The pupal stage lasts agement of mealybugs in vineyards. In: Bostanian NJ
et al (eds) Arthropod management in vineyard pests,
for an average of 2.50 days and the males trans-
approaches, and future directions, Springer Science+
form into winged adult forms. They undergo a Media B.V., Dordrecht, pp 271307. doi
radical change during their life cycle the wing- 10.1007/978-007-4032-7-12
less nymphs transform into winged adults. The Jayanthi R (1986) Mealybugs. In: David H, Easwaramoorthy
S, Jayanthi R (eds) Sugarcane entomology in India.
adult female body is oval, whitish, wingless and
Sugarcane Breeding Institute, Coimbatore, pp 259275
sparsely covered with white mealy substance. The Kamariya NM, Patel VN (2011) Biology of mealy bug,
length and width of adult females are 867.19 m Phenacoccus solenopsis (Tinsley) on cotton. J Cotton
and 368.88.78 m, respectively. After mating, the Res Dev 25(1):115118
Kim SC, Song J-H, Kim D-S (2008) Effect of temperature
adult females secrete an ovisac of white waxy sub-
on the development and fecundity of the Cryptic
stance in about 714 h and egg laying begins 37 h Mealybug, Pseudococcus cryptus, in the laboratory.
after this process. The eggs are laid in a bead- J Asia-Pacic Entomol 11(3):149153
shaped pattern, but later they are found in a disar- McKenzie HL (1967) Biology (Life history, Annual
Successions) morphology and classication.
rayed and scattered manner under mealy covering.
Mealybugs of California. University of California
Oviposition is completed in about 38 h with a Press, pp 2427, 3640
maximum fecundity of 79 eggs and the females Milena Varela A, Belloti AC (1981) Some aspects of the
are not able to survive more than 4 h after egg lay- biology of and observations on a new mealybug of
cassava Phenacoccus herreni (Homoptera:
ing. At 32.2235.10 C and 5565 % humidity, all
Pseudococcidae) in Colombia. [Spanish]. Revista
the eggs hatch after about 69 days of incubation. Colombiana de Entomologia 7(1/2):2126
Mishra D, Mukhopadhyay AK, Pramanik A (2004)
Biology of the mealybug Phenacoccus bengalensis
Pramanik and Ghose, 1999 (Homoptera:
References Pseudococcidae). Uttar Pradesh J Zool
Addis T, Azerefegne F, Blomme G, Kanaujia K (2008) Mukhopadhyay AK (2005) Study on the biology of the
Biology of the enset root mealybug, Cataenococcus mealybug, Ferrisicoccus psidii. Ann Plant Protect Sci
ensete and its geographical distribution in Southern 13(1):239240
Ethiopia. J Appl Biosci 8(1):251260 Nakahira K, Arakawa R (2006) Development and repro-
Alam S, Karim ANMR (1981) Rice mealybug, Brevennia duction of an exotic pest mealybug, Phenacoccus
rehi in Bangladesh. Bangladesh J Zool 9(1):1726 solani (Homoptera: Pseudococcidae) at three constant
Ali M (1995) Bionomics of sugarcane mealybug, temperatures. Appl Entomol Zool 41:573575
Kiritshenkella sacchari (Green) (Homoptera, Nikam ND, Patel BH, Korat DM (2010) Biology of inva-
Pseudococcidae). Pakistan J Zool 27(1):1519 sive mealy bug, Phenacoccus solenopsis Tinsley
Awadallah KT, Ammar ED, Tawk MFS, Rashad A (1979) (Hemiptera: Pseudococcidae) on cotton. Karnataka
Life-history of the white mealy-bug Ferrisia virgata J Agric Sci 23(4):649651
(Ckll.) (Homoptera, Pseudococcidae). Deutsche Pegoraro RA, Bellotti AC (1994) Biological aspects of
Entomologische Zeitschrift 26(1/3):101110 Pseudococcus mandio Williams (Homoptera:
Ayyar TVR (1939) The rice mealybug in South India. Pseudococcidae) in cassava [Portuguese]. Anais da
J Mysore Agric Exp Union 17:179188 Sociedade Entomologica do Brasil 23(2):203207
106 M. Mani and C. Shivaraju

Pramanik A, Ghose SK (1993) Experiments on the biol- Sahoo AK, Ghosh AB, Mandal SK, Maiti DK (1999)
ogy of the brinjal mealybug, Coccidohystrix insolita Study on the biology of the mealybug, Planococcus
(green) (Pseudococcidae: Homoptera). Ann Entomol minor (Maskell) Pseudococcidae: Hemiptera).
11(1):1518 J Interacademicia 3(1):4148
Rajendra A (1974) The biology and control of Vennila S, Deshmukh AJ, Pinjarkar D, Agarwal M,
Saccharicoccus sacchari Ckll. (Hom: Pseudococcidae) Ramamurthy VV, Joshi S, Kranthi KR, Bambawale
the pink mealy bug of sugar cane in Sri Lanka. Ceylon OM (2010) Biology of mealybug, Phenacoccus
J Biol Sci 11(1):2328 solenopsis on cotton in Central India. J Insect Sci
Razak TA, Ananthi DV, Jayanthi R (1994) Biology of the 10:119
sugarcane mealybug, Dysmicoccus carens Williams Walton VM, Pringle KL (2005) Developmental biology of
(Homoptera: Pseudococcidae). J Entomol Res vine mealybug, Planococcus cus (Signoret)
18(2):169174 (Homoptera: Pseudococcidae), and its parasitoid
Saha A, Ghosh A (2001) Biological studies on the mealy- Coccidoxenoides perminutus (Timberlake)
bug, Nipaecoccus viridis (Newstead) on various host (Hymenoptera: Encyrtidae). African Entomol
plants. Uttar Pradesh J Zool 21(1):7578 13(1):143147
Culturing of Mealybugs
M. Mani and C. Shivaraju

Culturing of mealybugs is essential to rear the laboratory in different countries on potato tubers
natural enemies, particularly parasitoids and and cucurbit fruits for the purpose of mass breed-
predators for use in the eld. Biological control ing of their parasites and predators (Ahmad and
programmes of mealybug species have relied on Ghani 1970). Large-scale multiplication of the
sprouting potatoes, pumpkins and butternut for mealybug for mass production of natural enemies
rearing of both mealybugs and their natural ene- was done on potato sprouts and pumpkin (Ahmad
mies. The ability to mass-rear the mealybugs is a and Ghani 1970. The rearing of Ferrisia virgata
vital step towards the culturing and colonisation (Cockrell) on brinjal has been reported by Rawat
of its natural enemies. An inexpensive mass- and Modi in India.
rearing technique and a nutritionally efcient but
simple diet have to be developed for the mealy-
bugs. The nutritional regime should be capable of 7.1 Potato Sprouts
producing and supporting great numbers of
mealybugs at low cost. An important requirement The use of potato sprouts as an insectary host for
for mass-rearing substrate is a long shelf life, the mealybugs culture was discovered by H. S.
which obviates the regular provision of fresh Smith and E. J. Branigan of the State insectary of
food. In this regard, butternut, pumpkins and USA (Branigan 1916). It was later modied by
sprout in potatoes have been found as suitable Smith and Armitage (1920), who found that
substrates for the mass-rearing of mealybugs white sprouts which developed in subdued light
(Johnson and Giliomee 2011). and at temperatures of 21.122.2 C were highly
In the large-scale production of mealybugs, acceptable to the mealybugs (Fig. 7.1).
potato sprouts or ripe pumpkins have been used The production method of P. citri on potato
in several countries. For mass rearing, a pure cul- sprouts is described in detail, as given by Fisher
ture of Planococcus citrii (Risso) must be main- (1963). The variety Red Bliss Triumph is pre-
tained in an isolated room solely for infesting ferred to Bounty or White Rose because it pro-
work (Finney and Fisher 1964). Species of duces sturdy sprouts highly acceptable to the
mealybugs have been satisfactorily reared in the mealybug and its natural enemies.
Potatoes after harvest should be stored for
more than 3 months at 2.2 C. Fans have to be
M. Mani (*) C. Shivaraju
provided to facilitate the circulation of air, which
Indian Institute of Horticultural Research,
Bangalore 560089, India reduces the temperature uctuation throughout
e-mail: the storeroom, and also reduces the decay

Springer India 2016 107

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_7
108 M. Mani and C. Shivaraju

Fig. 7.1 Culturing of mealybugs on potato sprouts (Fisher 1963)

fostered by humidity. Planting trays are made of mum (properly bleached) potato sprouts.
redwood and their outside dimensions are Continuous weak light causes sprouts to become
18 4. Soil used is sandy silt, obtained from excessively etiolated and too much light causes
riverbed. Trays and soil can be sterilised prior to excessive leaf growth. Excessive long sprouts are
re-use. Approximately 3 months after harvest or pruned to 12 lengths. The time from planting
when sprouts begin to appear, the tubers are until infesting with mealybugs is usually 21 days
ready for planting. Medium to large-size sound in summer and 30 days in winter and in early
whole potatoes are used, and 2526 tubers are spring (Fig. 7.2).
placed about apart and on a layer of soil in Crawlers are removed from producing trays
the tray. They are covered with slightly damp- by allowing them to crawl into freshly cut short
ened soil. Immediately after planting, trays are leafy terminals of Switches of Pittosporus
placed on the racks of a thoroughly cleaned room undulatum placed among the sprouts. Schinus
and watered. Trays should be lled with brimful molle (California pepper) is also used in autumn.
of water every 4 or 5 days and watering should be Approximately 6 h after placing them on the
discontinued after the sprouts have been infested. trays of mealybugs, the switches are removed
Temperatures of 21.123.3 C appear to be opti- from the food room and placed on the fresh
mum for facilitating sprout growth and relative sprouts in the production from where the mealy-
humidity of 6084 % have given good results, bug crawlers move on to the sprouts as the
provided there is proper airow through the cul- switches dry out. During the transfer periods,
ture room. Control of light intensity in order to trays are not watered; light intensity is increased
minimise leaf growth and chlorophyll develop- and temperature is adjusted to 26.6 C. Another
ment is a critical factor in the production of opti- method is to remove every third tray in the row
7 Culturing of Mealybugs 109

Fig. 7.2 Mass production of mealybugs on potato sprouts

and replace it with a tray containing long sprouts preferred host for the mass rearing of Oleander
that can be carefully bent over to interlace with mealybug Paracoccus burnerae (Brain) (Johnson
the over-producing sprouts of adjoining trays. and Giliomee 2011).
Stock from one mealybug tray will infest from 20 In India, the rearing of mealybugs on potato
to 25 trays. The optimum temperature for con- sprouts has been standardised by Joshi. The fol-
tinuous culture of mealybugs lies between 20 and lowing are the steps involved: (1) Procurement of
23.8 C (Fisher 1963). Sprouting potatoes are the medium-sized potatoes with well-developed
110 M. Mani and C. Shivaraju

eyes. (2) Cleaning with tap water and keeping in Cucurbita maxima Gil. (Mineo 1967). The prop-
a basin lled with sterilised sand. (3) Covering agation of citrus mealybugs on ripe pumpkins, C.
potatoes with sand and water moderately. (4) moschata D., has been outlined by Chacko et al.
Within a week or two, the sprouts grow to a (1978) and Singh (1978). The pumpkins with
length of 34 in.. (5) Removing the potatoes from ridges and grooves and a small stalk are selected,
sand and washing them with tap water. (6) which makes the handling easy. To prevent rot-
Keeping them in sunlight for a day so that the ting, the pumpkins are treated with 0.1 % beno-
sprouts turn green. (7) Infesting one sprout with myl (1 g/L). The wounds, if any on the pumpkin,
ve gravid females of mealybug. (8) Keeping are plugged with melted parafn wax. Ovisacs on
infested potatoes at 27 C and 5060 % relative P. citri /M. hirsutus are distributed over the pump-
humidity (R.H.). kin fruits or crawlers are dusted on the fruits. In
due course, the crawlers settle on all sides of the
pumpkin. The infested pumpkins are kept on
7.2 Pumpkin small tripod stands, which can be arranged in the
racks. In about a month, the mealybug population
The rearing of P. citri on cucurbits in USSR was covers the whole pumpkin. A temperature of 25
rst reported by Sysoev (1953). In Sicily (Italy), C is to be maintained in the rearing room
the mealybug P. citri was reared on pumpkin, (Chacko et al. 1978; Singh 1978) (Fig. 7.3).

Fig. 7.3 Rearing of mealybugs on pumpkins

7 Culturing of Mealybugs 111

7.3 Host Plants 7.4 Diets

The mealybugs are cultured on host plants. Initial Attempts were also made to rear the mealybugs
culturing is always done on natural host plants. on articial diet. Rearing the cassava mealybug,
Sometimes mass culturing is also done on the Phenacoccus manihoti, was done on a dened
host plants. A mass production protocol is avail- diet (Calatayud et al. 1998).
able for the production of papaya mealybug
Paracoccus marginatus Williams and Granara de
Willink on potato sprouts. However, it was very References
difcult to maintain potato plants in high-
temperature areas where spoilage of potatoes is a Ahmad R, Ghani MA (1970) A note on the rearing of
scale insects and mealybugs on potato tubers and
concern. Alternatively, a mass production tech-
cucurbit fruits. Tech Bull Commonw Inst Biol Control
nique has been developed using Hibiscus canna- 13:105107
binus for mass production of the papaya Branigan EJ (1916) A satisfactory method of rearing of
mealybug. Seeds were procured locally. Before mealybugs for use in parasite work. Calif State Hort
Comm Monthly Bull 5:304306
sowing, the seeds were spread on paper and
Calatayud PA, Delobel B, Guillaud J, Rahb Y (1998)
allowed to dry under sunlight for 13 h. Trays of Rearing the cassava mealybug, Phenacoccus manihoti
45 cm 30 cm 13 cm (l w h) with four to six on a dened diet. Entomol Exp Appl 86(3):325329
holes in the bottom to drain out excess water Chacko MJ, Bhat PK, Rao LVA, Deepak Singh MB,
Ramanarayan BP, Sreedharan K (1978) The use of the
were lled with a mixture of sand, soil and farm-
lady bird beetle, Cryptolaemus montrouzieri, for the
yard manure (1:1:1) up to 9 cm and H. cannabi- control of coffee mealybugs. J Coff Res 9:1419
nus seeds were sown for culturing the plants Finney CL, Fisher TW (1964) Culture of entomophagus
under laboratory conditions. The seeds started to insects and their hosts. In: DeBach PD (ed) Biological
control of insect pests and weeds. Chapman and Hall,
sprout within 2 days and attained a height of
London, pp 328353
40 cm within 2025 days, which is the suitable Fisher TW (1963) Mass culture of Cryptolaemus and
stage for infestation with papaya mealybug for Leptomastix, natural enemies of citrus mealybugs.
mass production purposes. Paracoccus margin- Bull Calif Agric Exp 797:39
Helen M, Chikkanna S, Balasaraswathi J, Ravikumar N,
atus, placed on 2025-day-old seedlings, was
Sakthivel N, Bindroo BB (2013) Hibiscus cannabinus
allowed to develop to the second instar, at which L. (Malvaceae) as an alternate host plant for mass-
time the plant was cut and transferred to plastic rearing of Paracoccus marginatus Williams and
containers having one thin layer of absorbent cot- Granara de Willink (Hemiptera: Pseudococcidae) and
their exotic parasitoids. In: Proceedings of 13th work-
ton covered with one layer of tissue paper. Based
shop of the IOBC Global working group on mass rear-
on the number of 2nd-instar mealybugs present, ing and quality assurance, Bangalore, India, 68 Nov
parasitoids were released at a ratio of 2:1 (para- 2013, pp 3940
sitoid to mealybug) into each container after Johnson T, Giliomee JH (2011) Evaluation of citrus, but-
ternut and sprouting potatoes as mass rearing sub-
which the cage was covered with muslin cloth.
strates for oleander mealybug, Paracoccus burnerae
For production of 20,000 parasitoids on the (Brain) (Hemiptera: Pseudococcidae). Afr J Biotechnol
mealybug using potatoes, the approximate cost 10:83208344
was Rs. 8700, whereas culturing done on H. can- Mineo G (1967) Cryptolaemus montrouzieri. Observations
on morphology and bionomics. Bull Inst Ent Agric
nabinus would require about Rs. 6700. It is con-
Oss Fitopat Palermo 6:99143
cluded that culturing of papaya mealybugs on H. Singh SP (1978) Propagation of a coccinellid beetle for
cannabinus is easy, economical and suitable for the biological control of citrus and coffee mealybugs.
tropical conditions and allows more effective Scientic Conference, CPA, Dec 1978, 2 p
Smith HS, Armitage HM (1920) Biological control of
mass production of the mealybug and its parasit-
mealybugs attacking citrus. Calif Agric Exp Stn Bull
oids (Helen et al. 2013). 9:104158
Sysoev AT (1953) The possibility of combining biological
and chemical methods in the control of pests of agri-
cultural crops. Dok Vseseovuz Akad Selkhoz Nauk
Lenin 18:2631
Mode of Spread of Mealybugs
M. Mani and C. Shivaraju

Mealybugs spread through various means. Local

and short-distance dispersal of mealybugs is facili- 8.2 Trade and Commerce
tated by air currents, ant movements, farm labour-
ers and farm implements. Long-range dispersal/ Dispersal is likely to occur more rapidly over
movement of mealybugs is usually accomplished longer distances with the movement of infested
by transport of infested plant material. Cotton plants in trade. The rapid spread from one coun-
mealybugs have the propensity to spread through try to another is most likely to be due to move-
natural carriers such as raw cotton, linted cotton ment of mealybugs in trade. Both the obscure
seeds, wind, water, rain, birds, human beings, ants mealybug Pseudococcus viburni (Signoret) and
and farm animals. They have immense potential to the parasitoid are the new world species that
emerge as crop pests, thereby causing severe eco- coevolved in Chile and transported to Europe
nomic damage to a wide range of crops and pose a before the nineteenth century, arriving on the
grave threat to agriculture in the new area. roots and foliage of new world potatoes. The
spread of the papaya mealybug Paracoccus
marginatus Williams and Granara de Willink
8.1 Planting Material was also aided by the transport of the papaya
fruits infested with mealybugs from one state to
Infestations often begin with the purchase of another in India. Most of the invasive pests
infested plant material. The mealybug is pas- like Phenacoccus manihotti (Matile-Ferrero),
sively dispersed with the infested planting mate- Rastrococcus invadens Williams, Paracoccus
rial. Mealybugs are not noticed as they hide in marginatus etc. spread through the sale of plant-
protected sites, such as cracks and crevices in ing material, fruits or plants to other countries.
bark, leaf axils, root crowns, stems, under the
leaves and so on, when the population is very
low. The dispersal mechanism of rhizome- 8.3 Personnel
feeding root mealybugs is facilitated by the
movement of infested suckers. Plants with their associated insects must have
been carried to new areas by people for many
centuries, and people still carry the infested plant
M. Mani (*) C. Shivaraju
Indian Institute of Horticultural Research, material, as seen by numerous quarantine inter-
Bangalore 560089, India ception records.

Springer India 2016 113

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_8
114 M. Mani and C. Shivaraju

8.4 Irrigation Water 8.10 Ants

Root mealybugs spread through irrigation water Among the arthropods, ants have also been
from one spot to another. Besides, ood irriga- reported to disperse many mealybug species.
tion carries fallen leaves and other debris infested Ants are likely to carry the young mealybugs
with mealybugs from one spot to another. called as crawlers. Ants are known to transport
the mealybugs from plant to plant, between and
within elds, thus facilitating mealybug disper-
8.5 Air Currents sal. In California, it is often possible to see ant
Camponotus actually carrying the mealybugs
Some of the crawlers may be dispersed over lon- from its host plant, directly into the ants nest.
ger distances by air currents. Sticky trap collec- Ants are the primary or sole means of mealybug
tions revealed that Dysmicoccus neobrevipes dispersal in pineapple. Pheidole megacephala
Beardsley and D. brevipes (Cockerell) are dis- (F.) are seen carrying mealybugs from one pine-
persed by wind. In India, Paracoccus marginatus apple plant to another. The big-headed ant (P.
had spread very fast by wind dispersal of crawl- megacephala.), Argentine ant (Linepithema
ers from the state of Tamil Nadu to others. Aerial humile (Mayr)) and re ant (Solenopsis geminata
dispersal could be important in the colonization (F.)) are commonly found in the Hawaiian pine-
of mealybugs of new areas. apple agroecosystem, where they tend the mealy-
bugs for honeydew. These ants, especially P.
megacephala, have been blamed for dispersing
8.6 Animals mealybugs.

Mealybugs are known to cling to wild and domes-

tic animals. They get transported by the move- 8.11 Stage of the Mealybugs
ment of animals. and Dispersal

The female mealybugs being wingless and some

8.7 Transport even legless, are not highly vagile and always
have restricted distribution. Adult males and
The mealybugs clinging to the vehicles entering newly emerged rst-instar nymphs of most
from the infested orchards get transported to the mealybug species display active dispersal. Adult
other orchards. male mealybugs are winged. First-instar nymphs
(crawlers) have been found to possess numerous
characteristics that are considered as adaptations
8.8 Implements/Equipment for dispersal behaviour, including long legs and
antennae. After hatching, crawlers are very active
The dispersal of mealybugs is facilitated by farm and move to the upper leaves and tips of the plant,
implements/equipment during farm operations. and also from one plant to another. They move at
Harvesting equipment from the infested orchard a speed of 1.525 in. per minute. Other instars
carries the mealybugs from one place to another. remained immobile for the greater part of their
lives, infesting mainly the midrib, lateral veins
and growing points of the food plant. Only males
8.9 Farm Labourers of this insect have a winged life stage. First- and
second-instar nymphs of Pseudococcus longispi-
Farm labourers move from one orchard to nus (Targioni-Tozzetti) were found in sticky plate
another, especially at harvest time. Mealybugs traps erected around a commercial Josephine
are transported through their clothes, disposable pear block in Victoria, Australia. Of those
wares and shoes. trapped, 89 % were rst instars and 11 % second
8 Mode of Spread of Mealybugs 115

instars. Adult males are winged and capable of reducing the abundance of M. hirsutus with the
weak ight, but were caught on only 2 of the natural enemies, it would appear that many such
76 days of trapping. It is unlikely that the winged avenues for dispersal became ineffective.
males use the wind to assist them in dispersing to Presently, the spread of M. hirsutus is largely
new locations. Numbers of instars found in the limited to the transfer of mealybug life stages on
traps were positively related (p < 0.05) to the plants that are moved or especially ovisacs or
wind speed and to the square of the daily maxi- adult females on equipment. The cotton mealy-
mum temperatures. bug Ph. solenopsis was observed in 2006 and has
spread like wildre covering entire India within a
short time. Initially, hardly any parasitism was
8.12 Availability of Host Plant reported, but the absence of the parasitoid like
Aenasius bombawalei (later reported) aided in
Most of the mealybug species like spread of the mealybugs.
Maconellicoccus hirsutus (Green), Paracoccus
marginatus, Planococcus citri (Risso),
Nipaecoccus viridis (Newstead), Ferrisia virgata 8.14 Phoretic Method
(Cockerell), Phenacoccus solenopsis Tinsley,
Pseudococcus longispinus and Planococcus Reproductive females of the ant Acropyga epen-
lilacinus are highly polyphagous and known to dana Snelling participating in the ights are
attack hundreds of host plants aiding the spread known to carry the mealybug Rhizoecus colom-
of the mealybugs easily within the country. biensis (Hambleton) between mandibles indicat-
However, oligophagous cassava mealybug ing vertical transfer of mealybugs with their ant
Phenacoccus manihotti rst reported in 1973 hosts. Mealybugs and other scaled insects are
from Congo had become established in the whole known to cling to other insects like locusts and
cassava belt area by 1986, mainly due to the get dispersed during swarming. In another pho-
availability of cassava plants cultivated contigu- retic method, eggs and nymphs of Maconellicoccus
ously over a vast area in Africa. hirsutus were being transported by nymphs and
adult females of another mealybug, Ferrisia vir-
gata (Cockerell), in India.
8.13 Absence of Natural Enemies

There were several outbreaks of mealybugs. 8.15 Root Mealybugs

Mealybugs are usually well regulated by natural
enemies. Absence of natural enemies, particu- Under moist conditions, young root-mealybugs
larly in the case of invasive mealybugs, aids in or nymphs are active. They move short distances
the build-up of mealybugs and their spread rap- to adjacent plants. They may crawl from pot to
idly within the country. Most of the mealybugs pot via drainage holes. They are slow moving in
establish themselves easily in the new area and irrigation water, thereby facilitating the spread.
spread to the adjoining areas, in the absence of However, their dispersal potential is usually
naturally occurring predators, parasitoids and limited. Infestations often begin with the pur-
pathogens. Presence of natural enemies of M. hir- chase of infested plant material.
sutus has essentially stopped the natural spread
of the mealybug from the isolated desert region
to other areas of California. In 1999, millions of 8.16 Accidental Introduction
crawlers were produced per tree subject to an
array of methods of transport, including being The vine mealybug Planococcus cus (Signoret)
windblown or mechanically transferred by vehi- is an old world species that was accidentally
cles, trees, shrub pruning equipment, etc. By introduced into California in the early 1990s and
116 M. Mani and C. Shivaraju

then it quickly spread to all major grape-growing countries, causing severe damage. Since its
areas. The mango mealybug Rastrococcus accidental introduction into the island of Grenada
invadens Williams was accidentally introduced in in 1994, Maconellicoccus hirsutus, native of
Africa in the early 1980s from South East Asia South Asia, has been inexorably spreading
into Ghana and later spread to most of the African throughout several Caribbean islands.
M. Mani and C. Shivaraju

Mealybugs throughout the world cause a variety amino acids and other nitrogen compounds
of economic problems. The most obvious dam- (Franco et al. 2000; Gullan and Martin 2003;
age is caused by the sucking habits of these Silva and Mexia 1999; Tonkyn and Whitcomb
insects. The damage caused by the mealybugs is 1987). Thus, except for sucrose hydrolysis,
linked to sap intake. Heavy infestations often food digestion is hardly necessary. However,
cause stunting or death of the plant host. At times, organic compounds in phloem sap need to be
mealybugs have toxins and act as vectors of cer- concentrated before they can be absorbed, and
tain viruses detrimental to plant life. this occurs in the lter chamber, a specialized
component of the digestive system, which
enables the direct passage of water from the
9.1 Feeding Process anterior midgut to the Malpighian tubules,
and Endosymbionts thereby concentrating food in the midgut (Terra
and Ferreira 2003). The residue of ingested
Mealybugs are phloem feeders. As they feed, phloem sap, after digestion and assimilation in
they produce a sugary excretion (honeydew) the insect gut, is released from the anus as a
that supports the growth of sooty mould. sugar-rich material, the honeydew. Up to 90 %
Mealybugs feed by inserting their stylets of the ingested sugars may be egested in this
through the plant tissue to suck up sap from way (Mittler and Douglas 2003).
either phloem or mesophyll, or both. Males ter- Mealybugs have an obligatory association
minate their feeding towards the end of the sec- with prokaryotic endosymbionts, probably
ond nymphal stage. Generally, stylet because of the suboptimal nutrition furnished by
penetration is accomplished by the secretion of phloem sap, which lacks essential nutrients.
solidied saliva that forms a sheath around the These endosymbionts are believed to be
stylets. Similarly to other members of the sub- important for the nitrogen and sterol require-
order Sternorrhyncha, which includes scale ments of their hosts and may play a role in resis-
insects, aphids, psyllids and whiteies, mealy- tance to microbial pathogens or in detoxication
bugs consume a diet containing mainly carbo- of plant secondary compounds (Baumann 2005;
hydrates as well as limited amounts of free Gullan and Kosztarab 1997). Within their body
cavities, mealybugs have a structure, the bacteri-
M. Mani (*) C. Shivaraju ome, which comprises specialized cells, the bac-
Indian Institute of Horticultural Research, teriocytes, which harbour the primary
Bangalore 560089, India endosymbionts, that is, the P-endosymbionts

Springer India 2016 117

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_9
118 M. Mani and C. Shivaraju

(Kono et al. 2008; Thao et al. 2002). The in the eld. For example, the citrus mealybug has
P-endosymbionts have the unusual property of been found on plants from 70 botanical families,
containing prokaryotic secondary endosymbi- 60 % of which are characterized as non-woody
onts, the S-endosymbionts, within their cyto- plants, whereas on the international scale, this
plasm (von Dohlen et al. 2001). During male mealybug is a pest of subtropical and tropical
development, the bacteriome progressively crops, such as citrus, persimmon, banana and
degenerates in the prepupa and pupa, and became custard apple, or it damages various types of
almost unrecognizable in the adult male (Kono plant species in interior landscapes, greenhouses
et al. 2008). in particular. Another example of the apparent
contradiction between the long lists of host plants
and the narrow ranges of damaged crops is the
9.1.1 Host Plants case of Pseudococcus cryptus Hempel; although
this mealybug is known from 35 host plant fami-
The various species of plants and animals have lies (Ben-Dov 2006), in Israel it causes damage
characteristic climatic requirements for growth, only to citrus trees. Under low pressure of natural
survival and reproduction, requirements that enemies, for example, when they spread in new
limit their geographic distribution, abundance environments, mealybugs are observed on rela-
and interactions with other species (Gutierrez tively large numbers of host plants, in contrast
et al. 1993). Mealybugs feed on a variety of her- with the situation when there is effective biologi-
baceous and woody plants, including the angio- cal control.
sperm, gymnosperm and fern families. However,
most of the species with known hosts develop on Direct Damage
herbaceous plants, especially grasses (Poaceae) Mealybugs are phloem feeders that use long,
and composites (Asteraceae) (Ben-Dov 2006; slender mouthparts to suck out plant uids. Most
Kosztarab and Kozr 1988). As expected, infor- of the mealybugs can feed on the trunk, stem,
mation on the host ranges of mealybugs is mainly leaves, owers or fruits, and some on roots.
derived from observations of species of economic However, differences in the amount of damage
importance. Most species are apparently oligoph- caused by each species are often related to those
agous or stenophagous or monophagous, and factors that determine population size (e.g., num-
some are polyphagous (Ben-Dov 2006; Kosztarab ber of annual generations and female fecundity),
and Kozr 1988). However, such a characteriza- preferred feeding locations and temperature tol-
tion is problematic. Most of the economically erances. As the mealybugs feed, they excrete
important species are known to be associated carbohydrate-rich honeydew, which can accumu-
with long lists of hosts, and their performance late on the leaves and in the grape clusters, espe-
varies widely, ranging from development of high cially in late summer and early fall. The mealybug
population density, which eventually would kill icks honeydew away from its location, but it
the host plant, to poor development that renders still accumulates on the plant. It has long been
the survival of the population for several genera- noted that honeydew serves as a substrate for the
tions questionable. Plant growth conditions may development of sooty mould fungi that can result
strongly affect the success of the population: in further plant damage. For table-fruit growers,
under irrigation and fertilization, plant species any live or dead mealybugs and the honeydew or
become favourable hosts of mealybugs, whereas sooty moulds will cause cosmetic damage to fruit
in different environments the performance is usu- cluster and reduce its marketability. In most dried
ally poor. During laboratory studies, many of the fruits, juice and wine grapes, the contamination
mealybug pest species could be easily reared on from a small mealybug population, and the resul-
alternative hosts, such as potato sprouts or tant honeydew droplets, will not cause economic
squashes, which are not colonized by mealybugs damage. Although honeydew can be dissolved by
9 Damage 119

light rain and will dry in warm temperatures, problem to pineapple. Perhaps one of the most
when mealybug populations are severe, honey- important of these diseases is swollen shoot of
dew can accumulate to form a hard, wax-like cacao, transmitted by several mealybug vectors,
layer that covers the infested plant. A copious including Planococcoides njalensis (Laing) and
amount of honeydew gives the bark of the plant a Ferrisia virgala (Cockerell). This virus causes
water-soaked appearance. excessive damage to cacao trees each year.
Feeding damage can result in defoliation and,
after repeated annual infestations, cause vine
death. There are morpho-histological changes in 9.2 The Origin of Mealybug Pest
the plants due to the infestation of mealybugs on Status
plants like ramie (Boehmeria nivea), mulberry
(Morus alba), roselle (Hibiscus sabdariffa var. Similarly to other insect pests, mealybugs have
altissima) and mesta (Hibiscus cannabinus) diverse origins, including endemics, immigrants
infested with nymphs of Maconellicoccus hirsu- and mutants (Kim 1993). An indigenous species
tus (Green). Morphologically, linear growth of may become a serious pest: when a susceptible
the stem and petiole was arrested and their thick- crop species is introduced into the area, follow-
ness was increased. The leaf lamina was mark- ing environmental disturbance or as a result of
edly reduced and distorted. Histologically, the stress conditions. Invasive mealybug species
cells were enlarged and suffered reduced ligni- may attain pest status as soon as they success-
cation. There was an increase in the number of fully colonize a new territory, and affect nega-
stomata, which varied in the different plants. tively crop yield, which may happen when they
Mealybug (Rastrococcus invadens Williams) encounter a susceptible host, either local or
infestation of fruits caused a signicant reduction exotic. Planococcus citri (Risso) is an intro-
in weight and size of mango fruits, and also ash duced pest in most citrus-growing areas of the
content, crude bre and reducing sugars in Sri globe. It may weaken young citrus saplings, but
Lanka (Tobih et al. 2002). barely affects the growth of fruit-bearing trees;
the damage is mainly due to fruit infestation. Indirect Damage Two mealybug population trends were shown to
In most of the regions, the transmission of occur in citrus orchards in the Mediterranean
viruses, rather than mealybug feeding or contam- region (Franco et al. 2004): (1) outbreak dynam-
ination, is the primary concern. Several species ics, whereby the percentage of infested fruits
of mealybugs are vector-virus disease in crops (mainly by Pl. citri) typically increases expo-
like banana, blackpepper, grapevine, cocoa, pine- nentially, with maximal values higher than 30 %
apple, sugarcane etc. Severe infestations can being recorded during mid- to late summer, and
result in defoliation, cluster infestation and rot, as (2) non-outbreak dynamics, whereby the per-
shown for a Planococcus cus (Signoret) infesta- centage of infested fruits does not increase sig-
tion. There is a slight leaf chlorosis and phloem nicantly or, alternatively, exhibits only a small,
disruption. Grapevine leafroll virus infections relatively linear increase, with maximal values
impact the berry development and growth by lower than 30 %. Three major causes may lead
delaying budbreak, owering and berry matura- to mealybug outbreaks: (1) a recent invasion by
tion, including changes in colour, reduced sugar an exotic mealybug species, (2) the application
content and increased acidity in fruit juice. of non-selective pesticides, which disrupt the
Mealybug toxins are rather important in some biological balance, and (3) the effect of environ-
areas. The pineapple wilt in the Hawaiian Islands mental factors that might inuence the tritrophic
involves the pineapple mealybug, Dysmicoccus interactions among host-plant/mealybug/natural
brevipes (Cockerell), which is a serious economic enemies.
120 M. Mani and C. Shivaraju

These were subdivided by Franco et al. (2004) The mechanisms involved in these two types of
as follows: outbreaks were discussed by Hardin et al. (1995),
and studied by Franco et al. (2004) with regard to
1. Recent invasion by exotic mealybug species the mealybug pests of citrus. Environmental fac-
(a) Lack of control by natural enemies tors (Cause 3) may also directly and indirectly
2. Application of non-selective pesticides affect the tritrophic interactions that develop
(a) Mortality differences between pests and between mealybugs, their host plants and their
their natural enemies natural enemies, thereby initiating mealybug out-
(b) Indirect effects of pesticides on natural breaks. Several mechanisms may be involved.
enemies, for example, elimination of their Host-plant characteristics may favour or be detri-
prey mental to the development, reproduction and sur-
(c) Effects on predator and parasitoid host vival of mealybugs (Boavida and Neuenschwander
interactions 1995; Calatayud et al. 1994b; Leru and Tertuliano
(d) Trophobiosis positive indirect effects of 1993; Nassar 2007; Tertuliano et al. 1993;
pesticides on pests, mediated through Wysoki et al. 1977; Yang and Sadof 1995). The
changes in the host plant resistance mechanisms of the host plant may
(e) Hormoligosis positive direct effects of become involved in both the xation (antixeno-
pesticides on pests sis) and the development of the mealybug (anti-
(f) Effects of pesticides on insect behavior biosis) (Tertuliano et al. 1993). Tertuliano and
(g) Effects of pesticides on interspecic com- Leru (1992) concluded that the different levels of
petition among phytophagous species of resistance to the cassava mealybug, P. manhioti,
different taxa which were observed in different varieties of cas-
3. Effect of environmental factors (tritrophic inter- sava, were not associated with the concentrations
actions: host-plant/mealybug/natural enemy) of amino acids or sugars, with the ratios between
(a) Host-plant susceptibility and/or host- these concentrations, or with the compositions of
plant characteristics amino acids obtained from leaf extracts. The
(b) Water stress identication and assay of cyanogenic and phe-
(c) Nitrogen fertilization nolic compounds in the phloem sap of cassava
(d) Weather and the honeydew of the cassava mealybug were
(e) Mealybug defences, for example, carried out by Calatayud et al. (1994a). Yang and
encapsulation Sadof (1995) showed that variegation in Coleus
(f) Mealybug refuges from natural enemies blumei could increase the abundance of the citrus
Spatial refuge (cryptic behavior), for mealybug, P. citri. Sadof et al. (2003) found that
example, under the bark and on roots the life-history characteristics of P. citri on
Temporal refuge: ant interactions Coleus blumei were not correlated with total
Other factors that may affect natural ene- amino acids and sucrose contents in stem exu-
mies, for example, intraguild predation dates, but were correlated negatively with the
and interference, hyperparasitoids proportions of shikimic acid precursors and posi-
tively with those of other nonessential amino
Cause 1 is well documented with regard to acids. Host-plant characteristics can also inu-
mealybug outbreaks and is mainly driven by the ence the performance of the natural enemies of
combination of host susceptibility and absence of mealybugs (Serrano and Lapointe 2002; Souissi
natural enemies in the invaded region (Ben-Dov and Leru 1997; Yang and Sadof 1997). Water-
1994; Blumberg et al. 1999; Muniappan et al. stressed plants may favour the population
2006; Nakahira and Arakawa 2006; Roltsch et al. increases of mealybugs (Calatayud et al. 2002;
2006; Williams and Granara de Willink 1992). Gutierrez et al. 1993; Lunderstadt 1998).
The use of non-selective pesticides (Cause 2) Mealybug life-history parameters/damage
may lead to resurgence and secondary outbreaks. may also be inuenced by the levels of nitrogen
9 Damage 121

fertilization and leaf nitrogen concentration; high Blumberg D, Ben-Dov Y, Mendel Z (1999) The citriculus
mealybug, Pseudococcus cryptus Hempel, and its
nitrogen concentrations were shown to lead to
natural enemies in Israel: history and present situation.
enhanced performance of the citrus mealybug, P. Entomologica Bari 33:233242
citri (Hogendorp et al. 2006). The antibiotic Boavida C, Neuenschwander P (1995) Inuence of host
resistance of two varieties of cassava mealybug plant on the mango mealybug, Rastrococcus invadens.
Entomol Exp Appl 76:179188
increased with the addition of nitrogen (Leru
Calatayud PA, Rahbe Y, Delobel B, Khuonghuu F,
et al. 1994). Survival of immature sugarcane Tertuliano M, Leru B (1994a) Inuence of secondary
mealybugs, S. sacchari, increased to a maximum compounds in the phloem sap of cassava on expres-
at a soluble nitrogen concentration of 320 mg L1 sion of antibiosis towards the mealybug Phenacoccus
manihoti. Entomol Exp Appl 72:4757
in sugarcane, and decreased at higher levels,
Calatayud PA, Tertuliano M, Leru B (1994b) Seasonal
whereas mealybug size increased with increasing changes in secondary compounds in the phloem sap of
nitrogen concentration over the whole tested cassava in relation to plant genotype and infestation by
range (Rae and Jones 1992). Weather conditions, Phenacoccus manihoti (Homoptera, Pseudococcidae).
Bull Entomol Res 84:453459
especially temperature and relative humidity, are
Calatayud PA, Polania MA, Seligmann CD, Bellotti AC
major ecological factors that affect both mealy- (2002) Inuence of water-stressed cassava on
bugs and their natural enemies (Chong and Phenacoccus herreni and three associated parasitoids.
Oetting 2007; Gutierrez et al. 1993, 2008a; Entomol Exp Appl 102:163175
Chong JH, Oetting RD (2007) Intraguild predation and
Nakahira and Arakawa 2006). Encapsulation
interference by the mealybug predator Cryptolalemus
may adversely affect the degree of biological montrouzieri on the parasitoid Leptomastix dactylopii.
control exerted by mealybug parasitoids, as it Biocontrol Sci Tech 17:933944
may either prevent the establishment of exotic Franco JC, Silva EB, Carvalho JP (2000) Mealybugs
(Hemiptera, Pseudococcidae) associated with citrus in
parasitoids in new regions or reduce parasitoid
Portugal. ISA Press, Lisbon (in Portuguese)
efcacy (Blumberg 1997). The cryptic behavior Franco JC, Suma P, da Silva EB, Blumberg D, Mendel Z
and tending of mealybugs by ants may, respec- (2004) Management strategies of mealybug pests of
tively, originate spatial and temporal refuges citrus in Mediterranean countries. Phytoparasitica
from natural enemies. Several other factors may
Gullan PC, Kosztarab M (1997) Adaptations in scale
affect mealybugs natural enemies, which include insects. Annu Rev Entomol 42:2350
intraguild predation and interference (Chong and Gullan P, Martin JH (2003) Sternorrhyncha (jumping
Oetting 2007), and hyperparasitoids (Moore and plant lice, whiteies, aphids, and scale insects). In:
Resh VH, Card RT (eds) Encyclopedia of insects.
Cross 1992).
Academic, Amsterdam
Gutierrez AP, Neuenschwander P, Vanalphen JJM (1993)
Factors affecting biological control of cassava mealy-
References bug by exotic parasitoids a ratio-dependent supply-
demand driven model. J Appl Ecol 30:706721
Hardin MR, Benrey B, Coll M, Lamp WO, Roderick GK,
Baumann P (2005) Biology of bacteriocyte-associated
Barbosa P (1995) Arthropod pest resurgence: an over-
endosymbionts of plant sap-sucking insects. Annu
view of potential mechanisms. Crop Prot 14:318
Rev Microbiol 59:155189
Hogendorp BK, Cloyd RA, Swiader JM (2006) Effect of
Ben-Dov Y (1994) A systematic catalogue of the mealy-
nitrogen fertility on reproduction and development of
bugs of the world (Insecta: Homptera: Coccoidea:
citrus mealybug, Planococcus citri Risso (Homoptera:
Pseudoccocidae and Putoidae) with data on their geo-
Pseudococcidae), feeding on two colors of coleus,
graphical distribution, host plants, biology and eco-
Solenostemon scutellarioides L. Codd. Environ
nomic importance. Intercept, Andover
Entomol 35:201211
Ben-Dov Y (2006) Scales in a family/genus query.
Kim KC (1993) Insect pests and evolution. In: Kim KC,
Available at
McPheron BA (eds) Evolution of insect pests: patterns
chklist.exe?Family=Pseudococcidae&genus .
of variation. Wiley, New York
Accessed 14 Aug 2008
Kono M, Koga R, Shimada M, Fukatsu T (2008) Infection
Blumberg D (1997) Parasitoid encapsulation as a defense
dynamics of coexisting beta- and gammaproteobacte-
mechanism in the Coccoidea (Homoptera) and its
ria in the nested endosymbiotic system of mealybugs.
importance in biological control. Biol Control
Appl Environ Microbiol 74:41754184
122 M. Mani and C. Shivaraju

Kosztarab M, Kozr F (1988) Scale insects of Central Silva EB, Mexia A (1999) Histological studies on the sty-
Europe. Dr. W. Junk Publishers, Dordrecht let pathway, feeding sites and nature of feeding dam-
Leru B, Tertuliano M (1993) Tolerance of different host- age by Planococcus citri (Risso) (Homoptera:
plants to the cassava mealybug Phenacoccus manihoti Pseudococcidae) in sweet orange. Entomol Bari
Matile-Ferrero (Homoptera, Pseudococcidae). Int 33:347350
J Pest Manag 39:379384 Souissi R, Leru B (1997) Effect of host plants on fecun-
Leru B, Diangana J, Beringar N (1994) Effects of nitrogen dity and development of Apoanagyrus lopezi, an endo-
and calcium on the level of resistance of cassava to the parasitoid of the cassava mealybug Phenacoccus
mealybug P manihoti. Insect Sci Appl 51:8796 manihoti. Entomol Exp Appl 82:235238
Lunderstadt J (1998) Impact of external factors on the Terra WR, Ferreira C (2003) Digestive system. In: Resh
population dynamics of beech scale (Cryptococcus VH, Card RT (eds) Encyclopedia of insects.
fagisuga) (Hom., Pseudococcidae) in beech (Fagus Academic, Amsterdam
sylvatica) stands during the latency stage. J Appl Tertuliano M, Leru B (1992) Interaction between cassava
Entomol/Zeits Angew Entomol 122:319322 mealybugs (Phenacoccus manihoti) and their host
Mittler TE, Douglas AE (2003) Honeydew. In: Resh VH, plants amino-acid and sugar contents of sap. Entomol
Card RT (eds) Encyclopedia of insects. Academic, Exp Appl 64:19
Amsterdam Tertuliano M, Dossougbete S, Leru B (1993) Antixenotic
Moore D, Cross AE (1992) Competition between two pri- and antibiotic components of resistance to the cassava
mary parasitoids, Gyranusoidea tebygi Noyes and mealybug Phenacoccus manihoti (Homoptera,
Anagyrus mangicola Noyes, attacking the mealybug Pseudococcidae) in various hostplants. Insect Sci Appl
Rastrococcus invadens Williams and the inuence of a 14:657665
hyperparasitoid Chartocerus hyalipennis Hayat. Thao ML, Gullan PJ, Baumann P (2002) Secondary
Biocontrol Sci Technol 2:225234 (gamma-proteobacteria) endosymbionts infect the pri-
Muniappan R, Meyerdirk DE, Sengebau FM, Berringer mary (beta-proteobacteria) endosymbionts of mealy-
DD, Reddy GVP (2006) Classical biological control bugs multiple times and coevolve with their hosts.
of the papaya mealybug, Paracoccus marginatus Appl Environ Microbiol 68:31903197
(Hemiptera: Pseudococcidae) in the Republic of Tobih FO, Omoloye AA, Ivbijaro MF, Enobakhare DA
Palau. Fla Entomol 89:212217 (2002) Effects if eld infestation by Rastrococcus
Nakahira K, Arakawa R (2006) Development and repro- invadens Williams (Hemiptera; Pseudococcidae) on
duction of an exotic pest mealybug, Phenacoccus the morphology and nutritional status of mango fruits
solani (Homoptera: Pseudococcidae) at three constant Mangifera indica. Crop Prot 21:751761
temperatures. Appl Entomol Zool 41:573575 Tonkyn DW, Whitcomb RF (1987) Feeding strategies and
Nassar NMA (2007) Cassava genetic resources and their the guild concept among vascular feeding insects and
utilization for breeding of the crop. Genet Mol Res microorganisms. In: Harris KF (ed) Current topics in
6:11511168 vector research, vol 4. Springer, New York
Rae DJ, Jones RE (1992) Inuence of host nitrogen levels von Dohlen CD, Kohler S, Alsop ST, McManus WR
on development, survival, size and population- (2001) Mealybug beta-proteobacterial endosymbionts
dynamics of sugarcane mealybug, Saccharicoccus contain gamma-proteobacterial symbionts. Nature
sacchari (Cockerell) (Hemiptera, Pseudococcidae). 412:433436
Aust J Zool 40:327342 Williams DJ, Granara de Willink MC (1992) Mealybugs
Roltsch WJ, Meyerdirk DE, Warkentin R, Andress ER, of Central and South America. CABI, Wallingford
Carrera K (2006) Classical biological control of the pink Wysoki M, Izhar Y, Swirski E, Gurevitz E, Greenberg S
hibiscus mealybug, Maconellicoccus hirsutus (Green) in (1977) Susceptibility of avocado varieties to long-
southern California. Biol Control 37:155166 tailed mealybug, Pseudococcus longispinus (Targioni
Sadof CS, Neal JJ, Cloyd RA (2003) Effect of variegation Tozzetti) (Homoptera- Pseudococcidae), and a survey
on stem exudates of coleus and life history character- of its host plants in Israel. Phytoparasitica 5:140148
istics of citrus mealybug (Hemiptera: Pseudococcidae). Yang JS, Sadof CS (1995) Variegation in Coleus blumei
Environ Entomol 32:463469 and the life history of citrus mealybug (Homoptera:
Serrano MS, Lapointe SL (2002) Evaluation of host plants Pseudococcidae). Environ Entomol 24:16501655
and a meridic diet for rearing Maconellicoccus hirsu- Yang JS, Sadof CS (1997) Variation in the life history of
tus (Hemiptera: Pseudococcidae) and its parasitoid the citrus mealybug parasitoid Leptomastix dactylopii
Anagyrus kamali (Hymenoptera: Encyrtidae). Fla (Hymenoptera: Encyrtidae) on three varieties of
Entomol 85:417425 Coleus blumei. Environ Entomol 26:978982
Mealybugs as Vectors
R. Selvarajan, V. Balasubramanian,
and B. Padmanaban

Mealybugs are well-known sap-sucking insects 10.1 Feeding Behaviour

which transmit plant viruses. They are omnipres- of Mealybugs
ent, polyphagous, can cause more damage as
pests and are less uncommon as virus vectors. Mealybugs are found in moist and warm cli-
The feeding behavior of these vectors has pro- mates. They are less mobile on plants than other
found ecological and evolutionary implications groups of vectors, such as aphids and leaf hop-
for the viruses they transmit, as the acquisition pers, a feature that makes them relatively inef-
and inoculation of viruses occurs during vector cient as virus vectors. They spread from one plant
feeding. In most cases, there is an intimate rela- to another when in contact with them, and crawl-
tionship between the virus and its vector, and no ing nymphs move more readily than adults. Adult
transmissions occur without the insects feeding females can be extremely polyphagous and feed
in a specic manner. This feeding behavior often by sucking on plant sap. The stylet pathway to
causes considerable economic loss to agriculture the phloem is intercellular and contains several
through direct damage to crops and via virus intracellular punctures (Calatayud et al. 1994).
transmission (Golino et al. 2002; Miiler et al. These bugs have less control over ne stylet
2002). They are considered pests as they feed on movements than aphids and produce fewer
the plant juices of economically important crop (820/h) and longer intracellular punctures (20 s)
plants, and also act as vectors for several plant along the entire route to the phloem (Calatayud
viral diseases. The transmission of the plant virus et al. 1994; Cid and Fereres 2010). Mealybugs
species belonging to Caulimoviridae and rarely produce brief probes; they often reach the
Closteroviridae by different species of mealy- phloem after a single probe, and it takes a rela-
bugs is furnished in detail in this chapter. tively long time to reach the phloem. Some mealy
bugs are unable to tap into the phloem sieve ele-
ments even after a period of 20 h, but most are
able to reach the phloem in 16 h (Calatayud
et al. 1994; Cid and Fereres 2010). Mealybug sty-
lets are exceedingly long and are coiled within
R. Selvarajan (*) V. Balasubramanian their body when they are not feeding.
National Research Centre for Banana,
This unique morphology of their mouth may
Tiruchirapalli 620 102, India
e-mail: explain the propensity of mealybugs to make a
single stylet insertion and their inability to reach
B. Padmanaban
ICAR-National Research Centre for Banana, the phloem quickly, as is seen with other
Tiruchirappalli 620 102, India hemipterans. Once in the phloem, the mealybugs

Springer India 2016 123

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_10
124 R. Selvarajan et al.

may continue to feed from the same sieve tube aphid transmitted viruses; apparently, the virus is
for several days. Xylem ingestion is also a pre- carried on or near the stylets of the mealybug.
dominant feeding behavior for some mealybug
species (Calatayud et al. 1994; Cid and Fereres
2010). 10.3 Plant Viruses Transmitted
by Mealybugs

10.2 Types of Transmission 10.3.1 Viruses of Caulimoviridae

Mealybugs are phloem feeders, and a minimum Nineteen species of mealybugs belonging to 13
inoculation time of 15 min is needed for success- genera are known to occur on Musaceae (Watson
ful transmission. The virus persists through the and Kubiriba 2005). The Banana streak virus
moult, and for 23 days in starved or feeding vec- (BSVs) (Fig. 10.1a) is transmitted by Planococcus
tors. All mealybug-transmitted viruses appear to citri (Risso) and Saccharicoccus sacchari
have a semi-persistent mode of transmission (Cockerell), both of which colonize bananas
based on retention times; however, the Grapevine (Lockhart et al. 1992). Sugarcane bacilliform
leafroll-associated virus 3 (GLRaV-3) was found virus (SCBV) is serologically related to BSVs
in the salivary glands of its mealybug vector, (Lockhart and Autrey 1988), and is reported to be
suggesting a circulative mode of transmission transmitted from sugarcane to banana by
(Cid et al. 2007). Mealybug-transmitted viruses Saccharicoccus sacchari (Cockerell) (Lockhart
appear to have a high rate of acquisition and a and Olszewski 1993). Experimental transmission
low rate of inoculation (Cid and Fereres 2010). of BSVs has also been demonstrated with the
Ants that tend to carry the mealybugs may move pink pineapple mealybug Dysmicoccus brevipes
them from one plant to another (Sether et al. (Cockerell) (Kubiriba et al. 2001) and
1998), and occasionally, long-distance dispersal Pseudococcus comstocki (Kuwana) (Su 1998).
by wind may also occur. An important factor Ferrisia virgata (striped mealybug) (Fig. 10.1b)
contributing to the slow rate of spread is that has been found to be able to transmit the Banana
newly infected trees are not infective for some streak Mysore Virus (BSMYV) from banana to
weeks, or even months, and the virus may not banana (Selvarajan et al. 2006). Meyer et al.
become fully systemic in large trees for at least 1 (2008) reported that the transmission of activated
year. Temperature-mediated mealybug activity episomal Banana streak OL virus (BSOLV) to
may be an important variable in transmission cv. Williams banana (Musa sp.) by three mealy
efciency, and the virus spread can occur through bug species, viz. Dysmicoccus brevipes,
the airborne dispersal of young, GLRaV-3- Planococcus citri and P. cus.
infected crawlers (Cabaleiro and Segura 1997). Planococcus citri transmitted episomal
Cacao swollen shoot virus (CSSV) is transmitted BSOLV and the Banana streak GF virus
in a semi-persistent mode, meaning that the virus (BSGFV) from tissue-culture derived plants of
is taken up into the vector's circulatory system FHIA-4 to cv. Williams plants. Using FHIA-TC
but does not replicate within it (Dzahini-Obiatey 10 as the donor plant for transmission, the vector
et al. 2010). The feeding period required for the transmitted a 100 % episomal BSOLV to
acquisition of the virus is a minimum of 20 min, Williamss plants after 3 months, and the num-
but optimally 24 days (Posnette and Robertson bers of mealybugs feeding on individual recipi-
1950). Once acquired, the virus can be transmit- ent plants during the inoculation access period
ted within 15 min, but optimal transmission (IAP) ranged from 2 to 25 (Meyer et al. 2008).
occurs 210 h after acquisition. No transmission Episomal BSVs were transmitted by D. brevipes.
of the virus occurs through the mealybug eggs. At 3 months post transmission, the virus was
The relationship between the CSSV and mealy- detected and symptoms had appeared. Due to the
bugs has some similarities to the non- persistent reluctance of the mealybugs to move to Musa spp.,
10 Mealybugs as Vectors 125

a b c

e f g

h i j

Fig. 10.1 (a) Electron micrograph of BSV; (b) Ferrisia Electron micrograph of GVB; (g) Vine mealybug; (h)
virgata feeding on banana; (c) Pink pineapple mealybug, Symptoms of BSV in banana; (i) GLRaV infected grape-
Dysmicoccus brevipes; (d) Gray pineapple mealybug, D. vine; (j) Symptoms of mealybug wilt of pineapple
neobrevipes; (e) Electron micrograph of GLRaV; (f)

the low numbers survived the inoculation access et al. 2008). The fact that none of the mealybug
period; the virus was transmitted from the TC-5 species were able to transmit integrated BSOLV
to the William banana. However, no episomal from the FHIA-4 to Williams proves that the inte-
BSGFV could be transmitted by D. brevipes from grated form of BSV is not likely to be transmitted
the FH-4 donor to the recipient plants (Meyer by mealybugs; even highly efcient mealybugs
126 R. Selvarajan et al.

such as P. citri were unable to transfer any inte- PMWaV-2 infection and mealybug feeding are
grated viral sequences to the receptor plants. necessary for the development of mealybug wilt
Episomal BSV in tissue culture-derived tetra- disease (Hu and Sether 1999a, b; Sether and Hu
ploids is highly transmissible by efcient mealy- 2002a, b). All pineapple plants with wilt disease
bug vectors to Cavendish varieties. have PMWaV-2 infections, but not necessarily
Cocoa swollen shoot virus (CSSV), a badna- PMWaV-1 infections (Hu et al. 1997; Sether and
virus, is transmitted by at least 14 species of Hu 2002a). Several species of ants are associated
mealybugs of the family Pseudococcidae within with mealybugs (Beardsley et al. 1982; Carter
the Coccoidae (Roivainen 1976), but 1963). These ants assist in the establishment of
Planococcoides njalensis and Planococcus citri mealybug colonies, consuming the honeydew
are the most important vectors (Dongo and produced by the mealybugs (Petty and Tustin
Orisajo 2007). Piper Yellow Mottle Virus 1993), and can have a suppressive effect on the
(PYMV) is transmitted by the citrus mealybug, natural enemies of mealybugs (Jahn 1992).
Planococcus citri (Lockhart et al. 1997). Bhat Sether et al. (1998) reported that presence of ants
et al. (2003) reported that PYMV could easily be was correlated with an increased rate of virus
transmitted by the mealybugs (Ferrisia virgata) spread when caged with D. brevipes. All stages
from naturally diseased black pepper to healthy of D. neobrevipes acquire PMWaV, although
seedlings of black pepper. The initial symptoms vector efciency decreased signicantly in older
of the disease, like vein clearing and chlorotic adult females; the probability of a single third-
mottle, could be seen in 14 of the 20 test plants in instar immature transmitting the virus was 0.04.
5 weeks after inoculation. Macanawai et al. Both the species of the mealybugs acquired and
(2005) reported that the Taro bacilliform virus transmitted the PMWaV from infected pineapple
(TaBV) is transmitted by Pseudococcus material.
solomonensis. The Grapevine leafroll disease is caused by
grapevine leafroll-associated viruses (GLRaVs)
(Fig. 10.1e). These viruses are common in vine-
10.4 Viruses Belonging yards worldwide, and are often associated with
to Closteroviridae vitiviruses that are involved in the rugose wood
complex of grapevines. Ten mealybug species are
Mealybug-vectored viruses often exist as a com- known as vectors of one or several of these grape-
plex of viruses, such as the mealybug wilt of vine viruses, including the apple mealybug
pineapple complex, which is made up of three Phenacoccus aceris, which is widespread, and is
pineapple mealybug wilt-associated viruses able to transmit the Grapevine leafroll-associated
(PMWaV) (Sether et al. 1998, 2005; Sether and virus-1 and -3 (GLRaV-1 and -3). Vitiviruses,
Hu 2002a, b) and Grapevine leafroll-associated namely Grapevine virus A (GVA), Grapevine
viruses. Mealybug wilt of pineapple is a major virus B (GVB) (Fig. 10.1f), Grapevine virus D
constraint in the global production of pineapple (GVD) and Grapevine virus E (GVD), infect
(Carter 1934, 1942; Rohrbach et al. 1988; grape vines, and these are transmitted by the
Wakman et al. 1995). Carter (1934, 1942, 1949, members of several insect genera (Pseudococcus,
1962) found an association between mealybugs, Planococcus, Phenacoccus, Heliococcus,
particularly the pink pineapple mealybug, Neopulvinaria, Parthenolecanium, Cavariella
Dysmicoccus brevipes (Cockerell), (Fig. 10.1c) and Ovatus) in a semi-persistent manner (La
and the gray pineapple mealybug, D. neobrevipes Notte et al. 1997; Rosciglione et al. 1983; Garau
(Beardsley) (Fig. 10.1d), and wilt throughout the et al. 1995). Tsai et al. (2010; Le Maguet et al.
pineapple-growing regions of the world. 2012) studied the virusvector specicity analy-
PMWaV-1 infections are correlated with growth sis for mealybug transmission of GLRaVs. Plants
reductions of the plant crop (Sether and Hu infected with several GLRaVs virus species were
1998), and yield reductions in the ratoon crop. screened for vector transmission by the mealybug
10 Mealybugs as Vectors 127

Table 10.1 Mealybug transmitted plant viruses

Virus, genus and family Vector species Mode of transmission Reference
Banana streak virus sps, Dysmicoccus brevipes, Semi-persistent Meyer et al. (2008),
Badnavirus, Caulimoviridae Planococcus citri, Pl. cus, Kubiriba et al. (2001),
Pseudococcus longispinus, Selvarajan et al. (2006)
Ferrisia virgata
Sugarcane bacilliform virus Saccharicoccus sacchari Semi-persistent Lockhart et al. (1997)
sp. Badnavirus,
Piper yellow mottle virus; Planococcus citri Semi-persistent Lockhart et al. (1997),
Badnavirus, Caulimoviridae Pseudococcus elisae Bhat et al. (2003)
F. virgata
Taro bacilliform Badnavirus, Pseudococcus solomonensis Semi-persistent Macanawai et al.
Caulimoviridae (2005)
Schefera ringspot virus Planococcus citri Semi-persistent Lockhart and
(SRV) Olszewski (1996)
Cacoa swollen shoot virus, Planococcoides njalensis, Pl. Semi persistent Roivainen (1976)
Badnavirus, Caulimoviridae citri, F. virgata
Pineapple mealybug wilt Dysmicoccus brevipes Semi-persistent Sether et al. (1998)
associated virus-13; (Cockerell)
Closterovirus; Closteroviridae D. neobrevipes
GLRaV-1, 39; Ampelovirus, Heliococcus bohemicus, Semi-persistent Tsai et al. (2012)
Closteroviridae Phenacoccus aceris Signoret,
Planococcus cus
Pseudococcus longispinus,
Pseudococcus viburni,
Pseudococcus calceolariae,
Pseudococcus maritimus, Pl.
Grapevine virus A, B, D and Pseudococcus, Planococcus, Semi-persistent Garau et al. (1995), Le
E, Vitivirus, Betaexiviridae, Phenacoccus, Heliococcus Maguet et al. (2012)
Little Cherry Virus 2 Phenacoccus aceris Semi-persistent Raine et al. (1986)
Closterovirus, Closteroviridae

species Planococcus cus and Pseudococoucus (AAP) and peaked with a 24-h AAP, after which
longispinus. The results revealed that P. longispi- the transmission rate remained constant. In addi-
nus had transmitted the GLRaV-9 to the inocu- tion, the GLRaV-3 was found not to have been
lated plants, and showed that 18 % of the transovarially transmitted from infected females
inoculated plats were positive for GLRaV-9, but to their progeny (Table 10.1).
none of the inoculated plants were found positive Mealybugs are less mobile on the plant com-
for GLRaV-5, tested 9 months after the inocula- pared with groups of vectors such as aphids and
tion. Planococcus cus transmitted the GLRaV- leaf hoppers, a feature that makes them relatively
1,3,4,5,9 and GVA. This study showed that there inefcient as virus vectors. Mostly, the mealybug-
was no evidence of mealybugGLRaV specic- transmitted viruses appear to have a semi-
ity. Tsai et al. (2008) reported that the vine persistent mode of transmission based on
mealybug (Planococcus cus) (Fig. 10.1g) trans- retention times. Mealybug-transmitted viruses
mits GLRaV- 3 in a semi-persistent manner. First appear to have a high rate of acquisition and low
instars were more efcient vectors than adult rate of inoculation. Mealybug-vectored viruses
mealybugs, but the GLRaV-3 transmission lacked often exist as a complex of viruses, such as the
a latent period in the vector. Virus transmission mealybug-associated viruses. Badnaviruses such
occurred with a 1-h acquisition access period as PYMV, BSVs TaBV and CSSV have been
128 R. Selvarajan et al.

shown to transmit by different mealybug species. 34 years (Fig. 10.1j) (Crowdy and Posnette
In all of these studies, the interaction of the 1947). The impact of mealybug feeding and
mealybug vector with the virus and the host is Pineapple mealybug wilt associated virus-1
lacking; hence it is necessary to generate funda- (PMWaV-1), PMWaV-2 infection on pineapple
mental knowledge about the interaction of the yield and the spread of PMWaV-1 and mealybug
vector, the host and the virus system to develop wilt of pineapple (MWP) were evaluated under
effective disease management strategies for viral eld conditions; the results showed a 35 % reduc-
diseases. Epidemiological studies are also tion in yield when compared with PMWaV-free
required to predict the spread of the plant viruses plants (Sether and Hu 2002b). If MWP develops
through mealybugs, and the changing climatic during the rst 3 months of the plant crop, it can
conditions need to be considered while develop- lead to a 55 % reduction in average fruit weight,
ing forecasting models of disease spread. compared with fruits from PMWaV-free plants.

10.5 Loss Due to Mealybug- 10.6 Management

Transmitted Virus Diseases
The best way to manage the virus diseases trans-
Comprehensive analysis of yield loss due to mitted by mealybugs is to ensure that purchase of
mealybug infection has not been carried out in planting material is from virus-tested and virus-
many of the crops, however, the infection of free mother plants, and the control of
mealybug-transmitted viruses leads to drastic vectors mealybugs.
yield losses have been reported. Estimated yield
losses of between 7 % and 90 % have been attrib-
uted to the banana streak disease in different References
parts of the world (Harper et al. 2004; Lockhart
et al. 1998; Davis et al. 2000; Daniells et al. Beardsley JW Jr, Su TH, McEwen FL, Gerling D (1982)
Field investigations on the interrelationships of the
2001). In India, a yield loss of 49.48 % has been
big-headed ant, thegray mealybug, and pineapple wilt
recorded in cv. Poovan (Mysore, AAB) due to disease in Hawaii. Proc Hawaii Entomol Soc
BSV (Fig. 10.1h) (Thangavelu et al. 2000). In 24:5167
banana, the yield loss due to BSV is inuenced Bhat AI, Devasahayam S, Sarma YR, Pant RP (2003)
Association of a badnavirus in black pepper (Piper
by the cultivar, the virus species infecting, and
nigrum L.) transmitted by mealybug (Ferrisia virgata)
environmental conditions. Grapevine leafroll dis- in India. Curr Sci 84(12):15471550
ease occurs in all the major grape-growing Cabaleiro C, Segura A (1997) Field transmission of grape-
regions of the world, causing reductions in pro- vine leafroll associated virus 3 (GLRaV-3) by the
mealybug Planococcus citri. Plant Dis 81:283287
ductivity and quality of both wine and table
Calatayud PA, Rahbe Y, Tjallingii WF, Tertuliano M, Leru
grapes. B (1994) Electrically recorded feeding-behavior of
Infected grapevines (Fig. 10.1i) result in cassava mealybug on host and nonhost plants. Entomol
reduced berry yields, delayed maturity and poor Exp Appl 72:219232
Carter W (1934) Mealybug wilt and green spot in Jamaica
pigmentation. Estimated yield losses of as much
and Central America. Phytopathology 24:424426
as 3040 % due to Grapevine leafroll disease has Carter W (1942) The geographical distribution of mealy-
been recorded (Maree et al. 2013). In addition, bug wilt with notes on some other insect pests of pine-
the disease agent has been implicated in certain apple. J Econ Entomol 35:1015
Carter W (1949) Insect notes from South America with
types of graft incompatibility and young vine
special reference to Pseudococcus brevipes and
failure. Cacao swollen-shoot virus (CSSV) mealybug wilt. J Econ Entomol 42:761766
infects cacao trees and has a major effect on crop Carter W (1962) Insects in relation to plant disease. Wiley,
yields. Within 1 year of infection by CSSV, the New York, pp 238265
Carter W (1963) Mealybug wilt of pineapple: a reap-
yield decreases by 25 % and by 50 % within 2
praisal. Ann N Y Acad Sci 105:741764
years. The infected trees are usually killed within
10 Mealybugs as Vectors 129

Cid M, Fereres A (2010) Characterization of the probing to grapevine by Phenacoccus aceris. Phytopathology
and feeding behavior of Planococcus citri (Hemiptera: 102:717723
Pseudococcidae) on grapevine. Ann Entomol Soc Am Lockhart BEL, Autrey JC (1988) Occurrence in sugarcane
103:404417 of a bacilliform virus related serologically to banana
Cid M, Pereira S, Cabaleiro C, Faoro F, Segura A (2007) streak virus. Plant Dis 72:230233
Presence of Grapevine leafroll-associated virus 3 in Lockhart BEL, Olszewski NE (1993) Serological and
primary salivary glands of the mealybug vector genomic heterogeneity of banana streak badnavirus:
Planococcus citri suggests a circulative transmission implications for virus detection in Musa germplasm.
mechanism. Eur J Plant Pathol 118:2330 In: Proceedings of international symposium on genetic
Crowdy SH, Posnette AF (1947) Virus diseases of cacao improvement of bananas for resistance to diseases and
in West Africa. II Cross-immunity experiments with pests, Montpellier (FRA), 1992/09/7-9. Breeding
viruses 1A, 1B, 1C. Ann Appl Biol 34:403411 banana and plantain for resistance to diseases and
Daniells JW, Geering ADW, Bryde NJ, Thomas JE (2001) pests. CIRAD-FLHOR, Montpellier, pp 105113
The effect of Banana streak virus on the growth and Lockhart BEL, Olszewski NE (1996) Schefera ringspot
yield of dessert bananas in tropical Australia. Ann virus, a widely distributed mealybug-transmitted bad-
Appl Biol 139:5160 navirus occurring in Schefera and Aralia. Acta Hortic
Davis RI, Geering ADW, Thomas JE, Gunua TG, 432:196200
Rahamma S (2000) First records of Banana streak Lockhart BEL, Autrey LJC, Comstock JC (1992) Partial
virus on the island of New Guinea. Aust Plant Pathol purication and serology of sugarcane mild mosaic
29:281 virus, a mealybug transmitted closterolike virus.
Dongo LN, Orisajo SB (2007) Status of cocoa swollen Phytopathology 82:691695
shoot virus disease in Nigeria. Afr J Biotechnol Lockhart BEL, Kiratiya-Angul K, Jones P, Eng L, De
6:20542061 Silva P, Olszewski NE, Deema N, Sangalang J (1997)
Dzahini-Obiatey H, Domfeh O, Amoah FM (2010) Over Identication of Piper yellow mottle virus, a mealybug-
seventy years of a viral disease of cocoa in Ghana: transmitted badnavirus infecting Piper spp. in south-
from researchers perspective. Afr J Agric Res east Asia. Eur J Plant Pathol 103:303311
5:476485 Lockhart BEL, Ndowora TC, Olszewski NE, Dahal G
Garau R, Prota VA, Boscia D, Fiori M, Prota U (1995) (1998) Studies on integration of banana streak
Pseudococcus afnis mask., new vector of grapevine Badnavirus sequences in Musa: identication of
trichoviruses A and B. Vitis 34:6768 episomally-expressible badnaviral integrants in Musa
Golino DA, Sim ST, Gill R, Rowhani A (2002) California genotypes. In: Frison EA, Sharrock SE (eds) Banana
mealybugs can spread grapevine leafroll disease. Calif streak virus: a unique virus-Musa interaction?
Agric 56:196201 Proceedings of workshop of the PROMUSA Virol.
Harper G, Hart D, Moult S, Hull R (2004) Banana streak Working group held in Montpellier, France, 1921 Jan
virus is very diverse in Uganda. Virus Res 1998
100:5156 Macanawai AR, Ebenebe AA, Hunter D, Devitt LC,
Hu JS, Sether DM (1999a) Etiology of mealybug wilt of Hafner GJ, Harding RM (2005) Investigations into the
pineapple. In: Abstracts in Xth international congress seed and mealybug transmission of Taro bacilliform
of virology. Sydney, Australia, p 321 virus. Aust Plant Pathol 34(1):7376
Hu JS, Sether DM (1999b) Mealybugs and pineapple Maree HJ, Almeida RP, Bester R, Chooi KM, Cohen D,
mealybug wilt associated virus are both necessary for Doljam VV, Fuchs MF, Golino DA, Jooste AE,
mealybug wilt (Abstr.). Phytopathology 89:S70 Martelli GP, Naidu RA, Rowhani A, Saldarelli P,
Hu JS, Sether DM, Liu XP, Wang M, Zee F, Ullman DE Burger JT (2013) Grapevine leafroll-associated virus
(1997) Use of a tissue blotting immunoassay to exam- 3. Front Microbiol 4:82. doi:10.3389/
ine the distribution of pineapple closterovirus in fmicb.2013.00082. 2013 Apr 16
Hawaii. Plant Dis 81:11501154 Meyer JB, Kasdorf GGF, Nel LH, Pietersen G (2008)
Jahn GC (1992) The ecological signicance of the big- Transmission of activated-episomal banana streak OL
headed ant in mealybug wilt disease of pineapple. PhD (badna) virus (BSOLV) to cv. Williams banana (Musa
thesis, University of Hawaii, Honolulu sp.) by three mealybug species. Plant Dis
Kubiriba J, Legg JP, Tushemereirwe W, Adipala E (2001) 92:11581163
Vector transmission of Banana streak virus in the Miiler JG, Daane KM, McElfresh JS, Moreira JA,
screen house in Uganda. Ann Appl Biol 139:3743 Malakar-Kuenen R, Guillen M, Bently WJ (2002)
La Notte P, Buzkan N, Choueiri E, Minafra A, Martelli GP Development and optimization of methods for using
(1997) Acquisition and transmission of grapevine sex pheromones for monitoring the mealybug
virus A by the mealybug Pseudococcus longispinus. Planococcus cus (Homoptera: Pseudococcidae) in
J Plant Pathol 78:7985 Californian vineyards. J Econ Entomol 95:706714
Le Maguet J, Beuve M, Herrbach E, Lemaire O (2012) Petty GJ, Tustin H (1993) Ant (Pheidole megacephala F.)-
Transmission of six ampeloviruses and two vitiviruses mealybug (Dysmicoccus brevipes Ckll.) relationships
130 R. Selvarajan et al.

in pineapples in South Africa. Acta Hortic cies of mealybug (Dysmicoccus spp.). Phytopathology
334:387395 88:12241230
Posnette AF, Robertson NF (1950) Virus diseases of cacao Sether DM, Melzer MJ, Busto J, Zee F, Hu JS (2005)
in West Africa. VI. Vector investigations. Ann Appl Diversity and mealybug transmissibility of ampelovi-
Biol 37:363377 ruses in pineapple. Plant Dis 89:450456
Raine J, McMullen RD, Forbes AR (1986) Transmission Su HJ (1998) First occurrence of Banana streak badnavi-
of the agent causing little cherry disease by the apple rus and studies on its vectorship in Taiwan. In: Banana
mealybug Phenacoccus aceris and the dodder Cuscuta streak virus: a unique virusMusa interaction?
lupuliformis. Can J Plant Pathol 8:611 Proceedings of the Workshop PROMUSA Virology
Rohrbach KG, Beardsley JW, German TL, Reimer NJ, Working Group, pp 2025
Sanford WG (1988) Mealybug wilt mealybugs and Thangavelu R, Selvarajan R, Singh HP (2000) Status of
ants on pineapple. Plant Dis 72:558565 banana streak virus and banana bract mosaic virus dis-
Roivainen O (1976) Transmission of cocoa viruses by eases in India. In: Singh HP, Chadha KL (eds) Banana:
mealy bugs (Homoptera: Pseudococcidae). J Sci Agric improvement, production and utilization. Proceedings
Soc Finl 48:433453 of the conference on challenges for banana production
Rosciglione B, Castellano MA, Martelli GP, Savino V, and utilization in 21st century, AIPUB, NRCB, Trichy,
Cannizzaro G (1983) Mealybug transmission of grape- India, pp 364376
vine virus A. Vitis 22:331347 Tsai CW, Chau J, Fernandez L, Bosco D, Daane KM,
Selvarajan R, Balasubramanian V, Padmanaban B, Almeida RPP (2008) Transmission of Grapevine
Sathaimoorthy S (2006) Vector transmission of banana leafroll-associated virus 3 by the vine mealybug
bract mosaic and banana streak viruses in India. In: (Planococcus cus). Phytopathology 98:10931098
Proceeding of International symposium on Tsai CW, Rowhani A, Golino DA, Daane KM, Almeida
Management of vector-borne viruses held at RPP (2010) Mealybug transmission of grapevine lea-
ICRISAT, Hyderabad, 710 Feb 2006, p 110 froll viruses: an analysis of virusvector specicity.
Sether DM, Hu JS (1998) Corollary analyses of the pres- Phytopathology 100:830834
ence of pineapple mealybug wilt associatedvirus and Tsai CW, Daugherty MP, Almaida RPP (2012) Seasonal
the expression of mealybug wilt symptoms, growth dynamics and virus translation of grapevine leafroll-
reduction, and/or precocious owering of pineapple associated virus 3 in grapevine cultivars. Plant Pathol
(Abstr.). Phytopathology 88:80 61:977985
Sether DM, Hu JS (2002a) Closterovirus infection and Wakman W, Teakle D, Thomas JE, Dietzgen RG (1995)
mealybug exposure are necessary for the development Presence of clostero-like virus and a bacilliform virus
of mealybug wilt of pineapple disease. Phytopathology in pineapple plants in Queensland. Aust J Agric Res
92:928935 46:947958
Sether DM, Hu JS (2002b) Yield impact and spread of Watson GW, Kubiriba J (2005) Identication of mealy-
Pineapple mealybug wilt associated virus-2 and mealy- bugs (Hemiptera: Pseudococcidae) on banana and
bug wilt of pineapple in Hawaii. Plant Dis 86:867874 plantain in Africa. Afr Entomol 13:3547
Sether DM, Ullman DE, Hu JS (1998) Transmission of
pineapple mealybug wilt-associated virus by two spe-
Economic Importance
M. Mani and C. Shivaraju

Mealybugs are widely distributed phytophagous discoloured welts on the rind of the fruit,
insects, often with broad host ranges. There are ower, etc.
approximately 2000 described mealybug species 2. Mealybugs excrete copious quantities of hon-
worldwide. According to Millar et al. (2002), 158 eydew, which is a substrate for the fungus,
species of mealybugs are recognized as pests. sooty mould. Sooty mould is black in colour
Mealybug is a pest, which can have a consider- and may stain the fruit/ower decreasing the
able negative economic impact on a wide range packout percentage as well as causing a delay
of crops and ornamentals. In the last 30 years, in fruit colour development. Photosynthetic
there have been several major outbreaks of potential, especially of young trees, may be
mealybugs causing alarming damage to crops, as negatively affected if sooty mould infection is
a result of invasion/accidental introductions. severe.
Losses and costs of controlling mealybugs in 3. Mealybug is a phytosanitary pest in some
Georgia (USA) in 1996 were estimated at about export markets (USA, Japan) and if found on
$9.8 million. Damage and costs of controlling the fruit/ower destined for these markets can
pink hibiscus mealybug in the United States were result in rejection of the consignment and
recently estimated at $700 million annually. In could place these important markets at risk for
South Africa, costs for control of vine mealybug the future.
in vineyards were estimated at around $100 per 4. Mealybugs act as vectors of plant virus dis-
hectare per season. Most notorious mealybug ease causing heavy losses. Several mealybugs
species are polyphagous, and have become seri- are responsible for transmission of Grapevine-
ous pests of different crops under different leafroll-associated virus (GLRaV), and the
environments. virus infection was predicted to spread with
Economic damage can happen in four ways: the economic impact of Grapevine-leafroll-
associated virus-3 (GLRaV-3) infection
1. A high population of mealybug can lead to exceeding 10,000 dollars per ha, annually in
fruit, ower/leaf drop, fruit/ower deforma- South Africa.
tion (high shoulders) and development of
Mealybugs spread between continents through
M. Mani (*) C. Shivaraju
international trade. In the United States, there are
Indian Institute of Horticultural Research,
Bangalore 560089, India 350 species of mealybugs. Approximately 70 %
e-mail: of the 66 mealybug species that are considered as

Springer India 2016 131

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_11
132 M. Mani and C. Shivaraju

pests are invasive. Invasive mealybugs in also known to transmit the virus known as cholo-
California are serious pests of several economi- rotic streak (Williams 2004). Birendracoccus
cally important crops. There are several other saccharifolii (Green) is a major pest of sugarcane
mealybugs that reveal the extent of damage and in India and a vector of spike disease (Ali 1962).
economic losses. In New Zealand, most of the Coccidohystrix insolita (Green) has been a seri-
known 114 species of mealybugs are found only ous pest of brinjal, egg plant/aubergine, in Bihar,
on native plants. Three cosmopolitan and inva- West Bengal, Tamil Nadu, Kerala and several
sive Pseudococcus species are frequently occur- other states in India (Williams 2004). Economic
ring pests of horticultural crops in the country, damage by mealybugs on brinjal was reported in
where they account for more than 99 % of the Pakistan and also in other Asian countries (Arif
mealybug fauna in orchards and vineyards et al. 2009).
(Charles 1993). In France, scale insects, includ- Dysmicoccus boninsis (Kuwana) is a wide-
ing mealybugs, represent 31 % (Streito and spread pest of sugarcane causing economic dam-
Martinez 2005) of the newly introduced species age (Ben-Dov 1994). Dysmicoccus brevipes
in recent years, although all mealybug pests on (Cockerell) is a well-known pest of pineapples
grapevine are native (Sforza 2008). Likewise, in worldwide and also coffee. It acts as vector of
many countries, there were serious economic pineapple wilt in Hawaii and several other coun-
losses caused by mealybugs. tries. It is one of the principal pests of mango in
Rhodesgrass mealybug, Antonina graminis Okinawa. D. brevipes was reported on oilpalm-
(Maskell), has been a major pest of many pasture infesting leaves, inorescence and ripe fruit
grasses and lawns, and to some extent on bam- bunches in India (Ponnamma 1999). Dysmicoccus
boos in various parts of the world. It had com- neobrevipes (Beardsley) is common in Hawaii
pletely destroyed thousands of acres of good and also in southern Asia. It has caused severe
pasture land. Injury is rst indicated by the stunt- loss to tube rose growers in India. Dysmicoccus
ing and reduction in the overall size of individual grassii (Leonardi) has been reported as a pest of
grass clumps, with darkening of the leaves and banana in Canary Islands (Beardsley 1964a, b)
eventual death of the host plant. Death of seed- and heavy infestations on plantain in Nigeria.
ling plants is known to occur in about 3 weeks. Ehrhornia cupressi (Ehrhorn) is a serious pest,
Conventional control is difcult because of the which caused the destruction of cypress hedges
position of the mealybug on its host. The success in California (Herbert 1920).
in controlling this mealybug in Texas is by the Gilli mealybug Ferrisia gilli (Gullan) is the
introduction of the parasitoid Neodusmetia sang- primary pest of pistachio covering over 3000
wani (Subba Rao) from India (Dean et al. 1979). acres of pistachios in California. It is also known
The cost of the control programme was estimated to attack and cause huge losses to a wide range of
at that time at $0.2 million, resulting in the sav- crops such as almonds, grapes, stone fruits.
ings of about US$200 dollars per annum. The striped mealybug Ferrisia virgata
Subsequently, colonies of the parasitoid have (Cockrell) has been of some concern to several
been sent elsewhere in the New World. Heavy countries. In the past few years, however, heavy
infestations of the mealybug Antonina pretiosa infestations were noticed on many ornamental
(Ferris) produce unsightly condition of the bam- plants. This has caused some alarm as this spe-
boo (McKenzie 1967). Brevennia rehi (Lindinger) cies is reported as an important pest, especially to
is an important pest of rice in India, Pakistan, cotton. It is found normally above ground on the
Burma, Indonesia, Bangladesh and some other foliage where it causes the usual honeydew-sooty
countries causing severe loss of the crop espe- mould-type damage. During severe weather con-
cially in the dry seasons. Grains from mealybug- ditions, in Africa at least, it may move to the
infested plants did not develop properly and that crown and roots of its host. This mealybug is
they tasted bitter, and if present in normal food, found on a wide range of hosts. It caused eco-
they spoilt the avour after being cooked. It is nomic losses to citrus, guava, custard apple,
11 Economic Importance 133

mango, cotton, pomegranate, pummelo, tuberose, to 100 % loss in grapevine and mulberry. It is also
pepper, jackfruit, poinsettia, Acalypha, known to attack other crop plants, guava, pome-
Caesalpinia, etc. in India (Mani and granate, custard apple, acid lime, Phalsa, hibis-
Krishnamoorthy 1993), as well as pepper in India cus, ber, sapota, okra, etc. in different countries.
and jute in Bangladesh. Formicococcus robustus Introduced natural enemies, mainly the parasit-
(Ezzat and McConnell) is only known from the oid Anagyrus kamali (Moursi) (already known in
Indian region but it is sometimes intercepted at the Old World) and Gyranusoidea indica (Shafee,
port inspection elsewhere. Although a polypha- Alam and Agarwal) and the predator
gous species, it is frequently found on mango, Cryptolaemus montrouzieri (Mulsant), have
and in Pakistan it is reported as a serious pest. brought the mealybug under control in Egypt,
Kiritshenkella sacchari (Green) is known to West Indies, the United States, etc.
cause severe loss to sugarcane growers in India. Maconelicoccus hirsutus was detected in teak
Another example that indicates the high eco- plantations in 2004 in the Banderas valley in
nomic importance of a polyphagous mealybug is Mexico. A biological control programme was
the pink hibiscus mealybug, Maconellicoccus initiated in May 2004 to release 210,000 of the
hirsutus (Green). This mealybug is indigenous to predator Cryptolaemus montrouzieri on 150 ha of
southern Asia, and actually is considered a poten- land. Damage to trees was reduced by 92 % (Villa
tially serious pest in the United States, because of Castillo 2006). Mizococcus sacchari (Takshashi)
its extremely broad range of economically impor- was very injurious to sugarcane in Taiwan
tant hosts, including citrus, ornamentals, vegeta- (Takahashi 1928). Its presence in European and
bles and the native American ora. It was rst Mediterranean Plant Protection Organization
reported in the Western Hemisphere in Hawaii in (EPPO) countries would probably affect export
1984, and later in Grenada in 1994; subsequently markets, since it is regulated as a quarantine pest
it has spread rapidly through the Caribbean by many countries in other continents.
islands and to southern California (1999) and Nipaecoccus viridis (Maskell) is widespread
Florida (2002). Without control, the economic throughout tropics and subtropics causing eco-
impact of M. hirsutus to U.S. agriculture has nomic losses to numerous crop plants including
been estimated at $750 million per year (Hall citrus, pomegranate, guava, grapes, ber, jackfruit,
et al. 2008). The same pink hibiscus mealybug mango, custard apple and pummelo in several
was introduced accidentally to the Caribbean counties. In India, it is a pest of stored potatoes.
area in 199394, and has since spread beyond, Cotton is often attacked, when gall-like swellings
eventually reaching the United States. This dam- appear on terminal shoots, and tea is often heav-
aging species was rapidly identied by taxono- ily infested. On Artocarpus spp., large aggrega-
mists such as Maconellicoccus hirsutus (Green); tions of the mealybug lead to drying of the shoots.
its biological control was described in detail by In South Africa, N. viridis is a major pest of cit-
Kairo et al. (2000), with discussion of the costs rus, and in Okinawa it is one of the principal pests
and benets. M. hirsutus is widely distributed of mango. When rst introduced into Jordan in
throughout southern Asia, Africa and other parts 1993, apparently without natural enemies, infes-
of the Old World including Australia. M. hirsutus tations sometimes resulted in total loss of the cit-
is reported as a vector of virus disease on cocoa rus crop. In Egypt, a severe outbreak of N. viridis
in Zanzibar and other plants in East Africa, which occurred on lebbak trees. Niapecoccus nipae
causes growth arrest and branch distortion (De (Makell) has become serious pest of avocado and
Lotto 1967). Maconellicoccus hirsutus gets guava in Hawaii (Zimmerman 1948) and Puerto
ranked as one of the most important polyphagous Rico (Martorell 1940). The species is now con-
mealybugs in southern Asia, especially in India trolled successfully in Hawaii by the parasitoid
still causing damage in parts of India (Mani et al. Pseudophycus uitilis (Timberlake). Nipaecoccus
2011). The pink hibiscus mealybug is a major nipae was also known to cause serious damage to
pest of grapevine in peninsular India causing up coconut in Bermuda (Bennet and Hughes 1959).
134 M. Mani and C. Shivaraju

Palmicultor palmarum (Ehrhorn) is reported calyxes of apple and pears grown for export has
to infest 5 % of coconut palms in Bangladesh and caused concern in Australia and New Zealand
India. The species attacks the spear leaves of oil (Ward 1966). Phenacoccus madeirensis (Green)
palm in India. It sometimes occurs deep in the is a common polyphagous mealybug in much of
brous material covering palm stems, where it is the New World, Africa and the Pacic region.
difcult for chemical insecticides to penetrate. This mealybug is injurious to potatoes (Solanum
Paracoccus marginatus (Williams and Granara tuberosum) in Peru, and the growth of associ-
de Willink) causes serious economic losses to the ated sooty moulds causes malformation and
tune of several crores of rupees to more than 90 damage to leaves of other plants in Japan,
plant species particularly to the papaya, tapioca where it has been reported recently. It has
and mulberry damage in more than 53 countries invaded India recently and found to be severe
including India. Paracoccus marginatus has on tapioca.
become a serious pest in the Caribbean islands, Phenacoccus manihoti (Matile-Ferrero)
where it attacks numerous plant species, espe- appeared on cassava in Africa in 1973, and soon
cially papaya. The mealybug has now reached the spread throughout the whole cassava belt. The
southern United States. The mealybug reached introduction of the parasitoid Apoanagyrus lopezi
Guam and Palau on C. papaya; these islands are (De Santis) from South America to Africa and
possible sources for future incursions into the the success of the biological control programme
Pacic area and southern Asia. Biological control against P. manihoti had been well documented by
of Pa. marginatus with Acerophagus papayae Herren and Neuenschwander (1991). The tre-
(Noyes and Schauff) saved the silk, papaya and mendous success is credited with preventing the
tapioca industry from the loss worth to 2000 malnutrition of millions of Africans and may
crores rupees in India alone (Mani and Shivaraju well be the most important example of classical
2012). Similar economic benets were realized biological control ever. Zeddies et al. (2001) cal-
in several other countries. Hatting (1993) reported culated the total costs and benets of this biologi-
Paracoccus burnerae (Brain) as the most impor- cal control programme for 27 African countries
tant pest on citrus in South Africa. over a 40-year period (19742013) under differ-
Phenacoccus aceris (Signoret) has become a ent scenarios, such as transport, loss of crop and
serious threat to apple, pear, plum and other fruit even the price of maize as a possible substitute.
trees in Miane, British Columbia, Nova Scotia, Based on the total cost of biological control at
California and South Africa. The parasitoid US$ 47 million, the benets from different sce-
Allotropa utilis (Muesbeck) was introduced to narios range mainly from 199:1 (or US$ 9.4 bil-
British Columbia where it became well estab- lion) to 430:1 (or US$ 202 billion). Although the
lished. This was considered one of the outstand- initial cost of identication of the mealybug was
ing successes of classical biological control. negligible, there was a taxonomic advantage in
Phenacoccus gossypii (Townsend and Cockerell) that the costs included funds set aside for a study
is widely distributed in many countries. It is a of the mealybugs of Central and South America
pest of numerous owering plants in nurseries by Williams and Granara de Willink (1992).
and greenhouses, and in natural environments. Phenacoccus manihoti remains a threat to the
This mealybug, which is most often found on the cassava in the areas of southern Asia, as does the
foliage of its host, apparently causes as much yellow cassava mealybug, P. herreni, which still
damage to its host plants. Phenacoccus solani causes problems in South America. Reduction of
(Ferris) has probably been introduced recently P. herreni populations is under way, mainly
and is now established in southern Asia. There through the introduction of the parasitoids
are reports that it is a pest of stored potatoes in Apoanagyrus diversicomis (Howard) and
North America, and heavy infestations have been Acerophagus coccois (Smith) (Bento et al. 1999).
found on tobacco in Zimbabwe. Presence of The most trenchant point concerning the parthe-
Phenacoccus graminicola (Leonardi) under the nogenetic species P. manihoti is that an outbreak
11 Economic Importance 135

could occur in southern Asia with the accidental Planococcus citri (Risso) is one of the most
introduction of just a single immature specimen. cosmopolitan mealybugs. It is considered a seri-
Phenacoccus solani (Ferris) and Ph. solenop- ous pest of citrus in many parts of the world dam-
sis (Tinsley) are examples of invasive pests of aging many other eld crops in tropics and
annual crops; they cause heavy damage to green subtropics as well as greenhouse in temperate
pepper in Israel and cotton in the Indian subcon- regions. The mealybug is known to attack mainly
tinent (Ben-Dov 2005; Hodgson et al. 2008; subtropical fruit trees and also olive under
Nakahira and Arakawa 2006). The damage Mediterranean climate conditions and ornamen-
caused by mealybugs is linked to sap uptake, tal plants in interior landscapes in cooler zones
honeydew secretion and associated sooty mould (Ben-Dov 1994; Franco et al. 2004). The citrus
development, toxin injection and virus transmis- mealybug has become a key pest in the mint and
sion, although the presence of the insects may tarragon industry in Israel. This cosmopolitan
itself lead to economic losses (Franco et al. 2000; species was probably the rst recorded as pest in
McKenzie 1967; Panis 1969). The cotton mealy- southern Asia. Chemical control of this insect is
bug, Phenacoccus solenopsis, native of the amazingly difcult. Planococcus citri is known
United States (New Mexico) invaded several to cause up to 38 65 % damage on various citrus
countries Central America, the Caribbean and species (sweet orange, acid lime and lemon),
Ecuador (Argentina, Brazil, Ghana, Colombia, pummelo, guava, grapes (60 % loss), ber, sapota,
Nigeria, Asia (Pakistan, India and China)). It is a pomegranate, custard apple, crossandra, coffee,
major pest posing a severe threat to the cotton etc. in India (Manjunath 1986; Mani 2001).
crop in India and vegetable growing areas of Biological control of P. citri with natural enemies
Thailand and several ornamental plants in many saved several citrus orchards in India, the United
countries. This mealybug caused economic dam- States, Italy, Australia and South Africa.
age in India and Pakistan reducing the yields up Planococcus is also listed as a vector of Ceylon
to 450 %. Phenacoccus solenopsis caused a loss cocoa virus in Sri Lanka and also Grapevine virus
of several lakhs of rupees to cotton growers in (GVA). Planococcus cus (Signoret) is a pest of
India alone. Phenacoccus gossypii (Townsend grapevine in the Mediterranean region, South
and Cockerell) is widely distributed in many Africa, Pakistan, Argentina, Georgia and
countries. It is a pest of numerous owering California, causing heavy losses to grape grow-
plants in nurseries and greenhouses, and in natu- ers. It also transmits the grapevine leafroll virus.
ral environments. This mealybug, which is most Planococcus kenyae (Le Pelley) is popularly
often found on the foliage of its host, apparently known as coffee mealybug. It has caused heavy
causes as much damage to its host as the citrus losses to coffee growers in Uganda, Tanzania and
mealybug, Planococcus citri (Risso). Heavy Kenya (Bigger 2009).
infestations of Ph. solani have been recorded on Planococcus lilacinus (Cockerell) is one of
tobacco in Zimbabwe. the most common in southern Asia and reports of
Phenacoccus saccharifolii (Green) is known damage vary. It is known to attack and cause seri-
to attack sugarcane in India, Nepal and Pakistan. ous economic losses to cocoa, guava, ber, citrus,
In Bihar (India), infestation causes leaves and black pepper, cashew, pomegranate, guava,
internodes to become drastically reduced so that sapota, coffee, chow chow, mango, etc. (Mani
the cane can resemble a spike. Young sugarcane 2001). Planococcus lilacinus is known to trans-
plants have been severely damaged by this spe- mit Ceylon cocoa virus in parts of Sri Lanka.
cies in West Bengal (India). Planococcoides Planococcus cus is a serious pest of grapevine
nijalensis (Laing) is the dominant vector of the in the Mediterranean region, South Africa,
cocoa swollen shoot virus in African countries. It Argentina, Georgia and Pakistan. It is also found
is also known to attack cashew, Annona, silk cot- transmitting GVA and grape leafroll virus (Ben-
ton, pineapple, Acacia, Albizia, Caesalpinia, Dov 1994; Daane et al. 2006; Zada et al. 2008).
Erythrina, coffee, Clerodendron, etc. Planococcus minor (Maskell) is a common
136 M. Mani and C. Shivaraju

species on economically important plats particu- a pest in greenhouses and nurseries, but is also
larly cocoa throughout its geographical range. found out of doors in warmer areas. It has been
Trees (Cupressus and Juniferus) infested with reported as a pest of avocados, grapes and citrus.
Planococcus ovae (Nasonov) suffer from dieback Severe infestations have been reported on black
of twigs, heavy accumulation of honey dew and pepper in India. The mealybug is a target pest for
decline of trees in Italy (Ben-Dov 1994). classical biological control in Australia, and the
Planococcus kraunhiae (Kuwana) is widely species has caused damage to avocados in Israel
spread in California, Taiwan, China, Japan dam- in recent years. It also acts as a vector of grape
aging fruit tress such as pears, grapes, persim- leafroll virus. The orchid mealybug Pseudococcus
mons, banana, citrus, gs, etc. Planococcus microcirculus (McKenzie) has caused many
minor Maskell is a common species of many eco- problems to orchid growers (McKenzie 1967). It
nomically important plants including cocoa. is found primarily on the roots of its host but
Planococcus ovae (Nasanov) is widely distrib- crawls to the foliage and leaf sheaths when infes-
uted in Neotropical and Palaearctic regions on tations become heavy. The type of damage is the
Anthurium, Cupress and Juniperus trees. Infested normal form of unsightly contamination with the
trees suffer from dieback. production of honeydew during heavy infesta-
Several members of the genus Pseudococcus, tions. Pseudococcus maritimus (Ehrhorn) is
for example, Ps. calceolariae (Maskell), Ps. lon- another species important primarily to grapes and
gispinus (Targioni-Tozzetti) and Ps. viburni pears in some countries. The presence of these
(Signoret), are important pests of apple, pear and mealybugs on the ripe marketed grapes results in
vineyards in New Zealand (Charles 1993), serious economic loss to the growers. Heavy
whereas around the Mediterranean they are con- infestations cause the grapes to crack, allowing
sidered mainly as pests of citrus, persimmon and mould contamination. Pseudococcus viburmi
several other subtropical fruits (Franco et al. (Signoret) is most common in tropical and tem-
2004). Pseudococcus comstocki (Kuwana) is a perate areas but it is not widespread in southern
serious pest on apple, mulberry, pears, peach in Asia. It may have been overlooked, however,
the United States and Japan. The citriculus owing to its cryptic habit of living on roots. In
mealybug, Pseudococcus cryptus (Hempel), is a Australia, it causes damage to lawns and tubers,
major pest of citrus in the east Mediterranean and is a target species there for classical biologi-
region, and it attacks coffee roots in Asia and cal control. It is causing damage to Californias
South America (Ben-Dov 1994; Williams and coastal vineyards.
Granara de Willink 1992). It is widespread and a Following the introduction of the cassava
polyphagous mealybug species and appears to be mealybug into Africa, another introduced mealy-
kept under control by natural enemies in southern bug Rastrococcus invadens (Williams) appeared
Asia. Citrus and coconut are its favourite host in West Africa in 198182, causing extensive
plants, and infestations are known to occur on oil damage to fruit trees including mango (Williams
palm in India. It is widely distributed in Southeast 1986b). This mealybug was already known from
Asia, Tropical Africa, Middle East Meditrranean India and Pakistan (Narasimham and Chako
and South America. It is particularly a pest of cit- 1988). Rastrococcus invadens is usually scarce in
rus in Israel and the pest was controlled with the parts of India because it is controlled by natural
introduction of Clausenia purpurea (Ishii). enemies. The introduction of the encyrtid
Pseudococcus fragilis (Brain) was rst found in Gyranusoidea tebyi (Noyes) from India to West
California and rapidly became a serious pest of Africa, and its swift control of the mealybug
citrus to the point that it threatened the industry; there, is hailed as another biological control suc-
it also became a serious pest in Abkhazia of cess (Neuenschwander et al. 1994). Rastrococcus
USSR. iceryoides (Green) is causing serious damage to
Pseudococcus longispinus (Targioni Tozzetti) mango from India, and other fruit trees, and it is
is distributed worldwide. This mealybug is often also a pest of cotton. At present, it is distributed
11 Economic Importance 137

throughout India and eastwards to Thailand and bug, but it has caused signicant damage to orna-
Malaysia. It has also reached East Africa, where mental bougainvillea plants in Britain, ruining
there have been reports of damage in inland parts their aesthetic appearance and reducing their
of Tanzania and Malawi. Rastrococcus iceryoi- market value. Large mealybug populations cause
des is also known to cause serious damage to necrosis of the foliage, leaf loss, dieback and
Kapok trees in Tanganyika. Saccharicoccus sac- moulds grow on the excreted honeydew.
chari (Cockerell) is distributed wherever sugar- Mealybug is a pest, which can have a consider-
cane is grown, particularly Hawaii, Egypt, able negative economic impact on a wide range
Somalia, Costa Rica, etc. In southern Asia, it has of crops and ornamentals.
been rated as one of the most important mealy- There are some ground-inhabiting mealybug
bugs attacking sugarcane, which is the main species of undetermined economic importance
source of sugar and alcohol. It is also a possible belonging to the genus Rhizoecus and Geococcus.
vector of rice diseases in Cuba and India. Puto pilosellae (Sulc) is a pest of strawberries
Spilococcus mamillariae (Bouche) is a common (Kosztarab and Kozar 1988). These species are
pest of ornamental succulent plants. almost impossible to control. They are capable of
Trionymus radicicola (Morrison) caused causing serious economic damage to some crops,
severe damage to sugarcane in Cuba when areas namely alfalfa, strawberry, banana, pepper, cof-
of sugarcane dried out due to heavy population of fee, etc. Rhizoecus americanus (Hambleton) is
the mealybug on the roots. Trionymus townesi often a serious pest in Florida nurseries and
(Beardsley) is also known to attack rice and sor- recently it appeared in Italy, where it infests orna-
ghum. In the Philippines, infested upland rice mental plants. Paraputo leveri (Green) has been
crops have been reported to show depressed recorded as damaging roots and killing coffee
areas; plants in these areas were apparently plants in Papua New Guinea (Williams 1986a).
stunted and yellowish. Vryburgia rimariae Paraputo theaecola (Green) is found on tea roots,
(Tranfaglia) is a pest of economic importance in apparently in large numbers in North India. It is
greenhouses in Italy. also a severe pest on the roots of Taraktogenos
One of the most common groups of insects kurzii, a plant that produces a valuable oil.
attacking ornamental plants is mealybugs. There Paraputo banzigeri sp. lives on the roots causing
are about 275 species of mealybugs known to be the death of Dimopcarpus longan. Paraputo
present in the continental United States. leveri (Green) is already known from much of the
Mealybugs are prevalent pests in greenhouses tropical Pacic region and southern Asia. In
and interior plantscapes such as shopping malls, Papua New Guinea, it is found on the roots of
conservatories, hotels and ofce buildings. coffee, where it is protected under a layer of the
Mealybugs cost growers and retailers millions of fungus Diacanthodes philippinensis and eventu-
dollars per year in control and crop damage or ally kills the trees.
loss. Damage is caused by mealybugs feeding on Rhizoecus cocois (Williams) is a hypogeal
host tissues and injecting toxins or plant patho- species known from India, where it occurs on
gens into host plants. In addition, mealybugs coconuts, causing roots to dry up and young
secrete a waste product, honeydew, which is a plants to show loss of vigour. Rhizoecus dianthi
syrupy, sugary liquid that falls on the leaves, (Green) is a serious pest of African violets in
coating them with a shiny, sticky lm. Honeydew California (Snetsinger 1966) and a major pest of
serves as a medium for the growth of sooty mould greenhouse plants in Europe. Rhizoecus kondonis
fungus that reduces the plants photosynthetic (Kuwana) is one of the most widespread and eco-
abilities and ruins the plants appearance. Feeding nomically important subterranean mealybugs in
by mealybugs can cause premature leaf drop, die- California, where it is a pest of alfalfa, prune
back and may even kill plants if left unchecked. trees and strawberry plants and also caused
There is almost no information published on the severe damage to citrus in Japan. Rhizoecus
economic importance of bougainvillea mealy- amorphophalli (Betrem) was recorded from
138 M. Mani and C. Shivaraju

Trivandrum, Kerala (India), on the roots of ele- Some mealybug species may be manipulated
phant foot yam, Amorphophallus sp., ginger, as benecial insects in conservation biological
Dioscorea and rhizomes of Curcuma domestica control tactics. For example, the cupress mealy-
stored for seed purposes. Rhizoecus amorpho- bug, Planococcus vovae (Nasonov), which
phalli sucks the cell sap from the tubers, and occurs on cupress trees (Cupressus spp.) grown
severely infested deformed tubers of elephant in windbreaks, serves as an alternative host for
foot yam, taro, tannia nd no place in the market, natural enemies of mealybug pests in surround-
nor do they accept for cooking, causing economic ing citrus orchards and cocoa plantations (Cox
loss in India. 1989; Ho and Khoo 1997; Franco et al. 2004).
Rhizoecus americanus (Ferris) is a soft- Mealybugs have been also used as benecial
bodied, sucking insect that attacks the tips of insects in biological control of weeds. For exam-
roots. It is very common in Florida and other ple, Hypogeococcus pungens (Granara de
southern states. However, if shipped in plants, it Willink) was successfully introduced from
continues to thrive indoors and in greenhouses. Argentina into Queensland (Australia) for the
These creatures are dangerous to plants and are control of Harrisia cactus (Eriocereus martini)
often ignored as insignicant or misidentied as and related plants (Williams and Granara de
mycorrhiza. Willink 1992). In southern Asia, Trabutina ser-
Geococcus coffeae (Green) is found through- pentina (Green) is conned to Tamarix spp. in
out most of southern Asia, often killing plants in Pakistan and India. Heavy infestations of the
several counties, where it has been introduced. mealybug cause withering of the plant, and the
Heavy infestations of Geococcus johorensis mealybug has the potential for biological control
(Williams) in Malaysia cause the yellowing and of Tamarix wherever the plants have gained weed
early dieback of the leaves. Xenococcus acropy- status. The mealybug Hypogeococcus festerianus
gae (Williams) was found causing damage to the has been used to control Harrisia cactus, a major
roots of grapes in India. weed in central Queensland.
Several mealybug species are vectors of viral Mealybugs have also provided food for
diseases of various crops: banana, black pepper humans; the biblical manna, one of the food
(Bhat et al. 2003), cocoa (Dufour 1991), grapevine sources consumed by the Israelites during their
(Tsai et al. 2008), pineapple (Sether and Hu 2002), wandering in the wilderness of Sinai, is believed
rice (Abo and Sy 1998) and sugarcane (Lockhart to have been the honeydew excretion of the
et al. 1992). In such cases, mealybugs may be eco- manna mealybug Trabutina mannipara
nomic pests even at low densities. For example, (Hemprich and Ehrenberg) (Ben-Dov 2006;
several mealybug species are responsible for Miller and Kosztarab 1979).
GLRaV-3 transmission to grapevine, which has
been shown by the strong positive correlations
between mealybug numbers and infection levels in References
the following season. The virus infection was pre-
dicted to spread rapidly within the vineyard, with Abo ME, Sy AA (1998) Rice virus diseases: epidemiol-
ogy and management strategies. J Sustain Agric
50 % infection occurring in years 6, 8 and 11 for
high, intermediate and low infection rates, respec- Ali SM (1962) Coccids affecting sugarcane in Bihar
tively. The economic impact of GLRaV-3 infec- (Coccidae: Hemiptera). Indian J Sugar Res Dev
tion in sensitive varieties exceeded $10,000 per ha 6:7275
Arif MI, Raq M, Ghaffar A (2009) Host plants of cotton
by years 7, 9 and 12, and protability was suf-
mealybug (Phenacoccus solenopsis): a new menace to
ciently affected to justify replanting by year 11 cotton agro ecosystem of Punjab, Pakistan. Int J Agric
(Walker et al. 2004). Transmission of pineapple Biol 11(2):163167
wilt by Dysmicoccus spp. and cocoa swollen shoot Beardsley JW (1964a) Notes on the pineapple mealybug
complex with descriptions of two new species
by Planococcoides njalensis (Laing) had resulted
(Homoptera, Pseudococcidae). Proc Hawaiian
in heavy crop loss in some countries. Entomol Soc 19:5568
11 Economic Importance 139

Beardsley JW (1964b) Notes on the pineapple mealybug Franco JC, Suma P, da Silva EB, Blumberg D, Mendel Z
complex, with descriptions of two new species (2004) Management strategies of mealybug pests of
(Homoptera: Pseudococcidae). Proc Hawaiian citrus in Mediterranean countries. Phytoparasitica
Entomol Soc XIX(1):5568 32:507522
Ben-Dov Y (1994) A systematic catalogue of the mealy- Hall DG, Roda A, Lapointe SL, Hibbard K (2008)
bugs of the world (Insecta: Homoptera: Coccoidea: Phenology of Maconellicoccus hirsutus (Hemiptera:
Pseudococcidae and Putoidae) with data on geograph- Pseudococcidae) in Florida based on attraction of
ical distribution, host plants, biology and economic adult males to pheromone traps. Fla Entomol
importance. Intercept Limited, Andover, 686p 91:305310
Ben-Dov Y (2005) The solanum mealybug, Phenacoccus Hatting V (1993) Mealybugs and cottony cushion scale on
solani Ferris (Hemiptera: Coccoidea: Pseudococcidae), citrus in South Africa. Citrus J 3:2022
extends its distribution range in the Mediterranean Herbert FB (1920) Cypress bark scale. Bull US Dep Agric
basin. Phytoparasitica 33:1516 Bureau Entomol Wash 838:122
Ben-Dov Y (2006) Scales in a family/genus query. Herren HR, Neuenschwander P (1991) Biological control
Available at of cassava pests in Africa. Annu Rev Entomol
chklist.exe? Family=Pseudococcidae&genus. 36:257283
Accessed 14 Aug 2008 Ho CT, Khoo KC (1997) Partners in biological control of
Bennet FD, Hughes IW (1959) Biological control of cocoa pests: Mutualism between Dolichoderus tho-
insect pests in Bermuda. Bull Entomol Res racicus (Hymenoptera: Formicidae) and
50:423436 Cataenococcus hispidus (Hemiptera: Pseudococcidae).
Bento JMS, de Moraes GJ, Bellotti AC, Castillo JA, Bull Entomol Res 87:461470
Warumby JF, Lapointe SL (1999) Introduction of par- Hodgson C, Abbas G, Arif MJ, Saeed S, Krar H (2008)
asitoids for the control of the cassava mealybug Phenacoccus solenopsis Tinsley (Sternorrhyncha:
Phenacoccus herreni (Hemiptera: Pseudococcidae) in Coccoidea: Pseudococcidae), an invasive mealybug
north-eastern Brazil. Bull Entomol Res damaging cotton in Pakistan and India, with a discus-
89(5):403410 sion on seasonal morphological variation. Zootaxa
Bhat AI, Devasahayam S, Sarma YR, Pant RP (2003) 1913:135
Association of a badnavirus in black pepper (Piper Kairo MTK, Pollard GV, Peterkin DD, Lopez VF (2000)
nigrum L.) transmitted by mealybug (Ferrisia virgata) Biological control of the hibiscus mealybug,
in India. Curr Sci 84(12):15471550 Maconellicoccus hirsutus Green (Hemiptera:
Bigger M (2009) A geographical distribution list of insects Pseudococcidae) in the Caribbean. Integr Pest Manag
and mites associated with coffee derived from litera- Rev 5:241254
ture published before 2010. Available at www.ipmnet- Kosztarab M, Kozar M (1988) Scale insects of Central Accessed 16 Europe. Akdeiai Kiado, Budapest, 456 p
July 2013 Lockhart BEL, Autrey LJC, Comstock JC (1992) Partial
Charles JG (1993) A survey of mealybugs and their natu- purication and serology of Sugarcane mild mosaic
ral enemies in horticultural crops in North Island, New virus, a mealybug-transmitted closterolike virus.
Zealand, with implications for biological control. Phytopathology 82:691695
Biocontrol Sci Tech 3:405418 Mani M (2001) Biological control of fruit crops. In:
Cox J (1989) The mealybug genus Planococcus Reddy PP, Verghese A, Krishna Kumar NK (eds)
(Homoptera: Pseudococcidae). Bull Br Mus Nat Hist Integrated pest management in horticultural ecosys-
(Entomol) 58:178 tems. Capital Publishsing Company, New Delhi,
Daane KM, Bentley WJ, Walton VM, Malakar-Kuenen R, pp 93107
Millar JG, Ingels CA, Weber EA, Gispert C (2006) Mani M, Krishnamoorthy A (1993) Bionomics and man-
New controls investigated for vine mealybug. Calif agement of the striped mealybug, Ferrisia virgata
Agric 60:3138 (Ckll.) A world review. Agric Rev 14:2243
De Lotto G (1967) A contribution to the knowledge of the Mani M, Shivaraju C (2012) Invasive papaya mealybug,
African Coccoidea, Homoptera. J Entomol Soc South Paracoccus marginatus and its biological control an
Afr 29:109120 overview. J Biol Control 26(3):201216
Dean HA, Schuster MF, Boling JC, Riherd PT (1979) Mani M, Krishnamoorthy A, Shivraju C (2011) Biological
Complete biological control of Antonina graminis in suppression of major mealybug species on horticul-
Texas with Neodusmetia sangwami (a classic exam- tural crops. J Hortic Sci 6(2):85100
ple). Bull Entomol Soc Am 25:262267 Manjunath TM (1986) Recent outbreaks of mealybugs
Dufour B (1991) Place and importance of different insect and their biological control. In: Jayaraj S (ed)
species in the ecology of Cssv (Cocoa swollen shoot Resurgence of sucking pests. Proceedings of national
virus) in Togo. Caf Cacao Th 35:197204 symposium, Tamil Nadu Agricultural University,
Franco JC, Silva EB, Carvalho JP (2000) Mealybugs Coimbatore, pp 249253
(Hemiptera, Pseudococcidae) associated with citrus in Martorell LF (1940) Some notes on forest entomology.
Portugal. ISA Press, Lisbon (in Portuguese) Carib For 1:2324
140 M. Mani and C. Shivaraju

McKenzie HL (1967) Mealybugs of California with tax- Streito JC, Martinez M (2005) Nouveaux ravageurs, 41
onomy, biology and control of North American spe- espces depuis 2000. Phytoma La Dfense des vg-
cies (Homoptera: Coccoidea: Pseudococcidae). taux 586:1620
University of California Press, Berkeley, 534 p Takahashi R (1928) Coccidae of Formosa. Philipp J Sci
Millar JG, Daane KM, McElfresh JS, Moreira JA, 36:327347
Malakar-Kuenen R, Guillen M, Bentley WJ (2002) Tsai C, Chan J, Fernandez L, Bosco D, Daane KM,
Development and optimization of methods for using Rodrigo RP (2008) Transmission of grapevine leaf
sex pheromone for monitoring the mealybug roll-associated virus 3 by the vine mealybug
Planococcus cus (Homoptera: Pseudococcidae) in (Planococcus cus). Phytopathology 98:S159
California vineyards. J Econ Entomol 95:706714 Villa Castillo J (2006) The use of biological control to
Miller DC, Kosztarab M (1979) Recent advances in the control forest pests in Mexico. [Spanish] El uso de
study of scale insects. Annu Rev Entomol 24:127 control biologico para el control de plagas forestales
Nakahira K, Arakawa R (2006) Development and repro- en Mexico. Forestal XXI 8:1112
duction of an exotic pest mealybug, Phenacoccus Walker JTS, Charles JG, Froud KJ, Connolly P (2004)
solani (Homoptera: Pseudococcidae) at three constant Leafroll virus in vineyards: modelling the spread and
temperatures. Appl Entomol Zool 41:573575 economic impact. Horticulture and Food Research
Narasimham AU, Chako MJ (1988) Rastrococcus spp. Institute of New Zealand Ltd, Mt Albert
(Hemiptera: Pseudococcidae) and their natural ene- Ward A (1966) Mealybugs (Hemiptera: pesudococcidae).
mies in India as potential biocontrol agents for R. Acta Entomol Sin 28:444446
invadens Williams. Bull Entomol Res 78:703708 Williams DJ (1986a) Scale insects (Hmoptera: coccoidea)
Neuenschwander P, Boavida C, Bokonon-Ganta Gado A, on coffee in Papua New Guinea. Papua New Guinea.
Herren HR (1994) Establishment and spread of J Agric For Fish 34:17
Gyranusoidea tebygi Noyes and Anagyrus mangicola Williams DJ (1986b) Rastrococcus invadens sp. n.
Noyes (Hymenoptera: Encyrtidae), two biological (Hemiptera: Pseudococcidae) introduced from the orien-
control agents released against the mango mealybug tal region to West Africa and causing damage to mango,
Rastrococcus invadens (Homoptera: Pseudococcidae) citrus and other trees. Bull Entomol Res 76:695699
in Africa. Biocontrol Sci Technol 4:6169 Williams DJ (2004) Mealybugs of southern Asia. The
Panis A (1969) Observations faunistiques et biologiques Natural History Museum/Southdene SDN. BHD,
sur quelques Pseudococcidae (Homoptera, Coccoidea) London/Kuala Lumpur, 896 p
vivant dans le midi de la France. Ann Zool Ecol Anim Williams DJ, Granara de Willink MC (1992) Mealybugs
1:211244 of Central and South America. CAB International,
Ponnamma KN (1999) Coccoids associated with oil palm Wallingford, 635 p
in India a review. The Planter 75(882):445451 Zada A, Dunkelblum E, Assael FJC, Silva EB, Protasov
Sether DM, Hu JS (2002) Closterovirus infection and A, Mendel Z (2008) Attraction of Planococcus cus
mealybug exposure are necessary for the development males to racemic and chiral pheromone baits: ight
of mealybug wilt of pineapple disease. Phytopathology activity and bait longevity. J Appl Entomol
92:928935 132:480489
Sforza R (2008) Les cochenilles sur la vigne. In: Les rava- Zeddies J, Schaab RP, Neuenschwander P, Herren HR
geurs de la vigne. Eds Feret, Bordeaux, pp 188210 (2001) Economics of biological control of cassava
Snetsinger R (1966) Biology and control of root feed- mealybugs in Africa. Agric Econ 24:209219
ing mealybugs on Saintpaulia. J Econ Entomol Zimmerman EC (1948) Homoptera: Sternorrhyncha.
59:10771078 Insect Hawaii 5:1464
M. Mani and C. Shivaraju

12.1 Macro-environmental this, for its only restriction is the distribution of

Preferences its host, Artemisia (Compositae). It is found in
high mountains at altitudes of 10,000 ft to low
Mealybugs are much more numerous than might coastal regions of 30 ft. It is also commonly
be expected. Most people know of them as com- found in dry chaparral areas.
mon garden and nursery pests, but few realize the
enormous native fauna which exist. Mealybugs
are found in areas ranging from the low moist 12.2 Microenvironmental
coastal regions to the high snow-covered areas. Preferences
They are found from elevations of 200 ft to alti-
tudes of over 12,000 ft above mean sea level. Do mealybugs show the wide diversity of host
They are found in salt marshes and hot, dry desert plants. The general groups of plants infested
sands. In these different environments, certain are perennial and annual owering plants
types of mealybugs are found more frequently (angiosperms), grasses, conifers and some
than others. In the very high altitude regions, ferns.
conifer- and perennial-inhabiting Puto and grass
sheath-infesting Trionymus are most likely to be
found. In the moist coastal regions, root- and 12.2.1 Perennial Flowering Plants
soil-inhabiting Rhizoecus and grass-infested
Trionymus are common. In the dry, arid deserts, Mealybugs are most commonly found in peren-
foliage- and root-inhabiting Phenacoccus and nial plants. In some regions, every possible niche
Spilococcus are numerous. These regions are not is utilized on the perennial hosts. In one instance,
restricted to the genera mentioned above, nor are in San Diego County, an Artemisia plant was
the genera restricted to just these regions infested with Rhizoecus gracilis McKenzie on
(McKenzie 1967). the roots, Phenacoccus antemisiae Ehrhorn on
There are some mealybugs which have no par- the crown, Spilococcus corticosus McKenzie
ticular environmental preference. Amonosterium under the bark and Amonostherium lichtensioides
lichtensioides (Cockerell) is a good example of (Cockerell) on the foliage. Perennial foliage-
infesting mealybugs, although common in the
M. Mani (*) C. Shivaraju eld, are predominately noticed in greenhouses
Indian Institute of Horticultural Research, and backyard gardens. On foliage and stems,
Bangalore 560089, India mealybugs apparently prefer tight, enclosed

Springer India 2016 141

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_12
142 M. Mani and C. Shivaraju

areas, for they are normally found in the leaf or yuccae (Coquillett) or Puto decorosus McKenzie
stem axils. Infestations on fruits are usually usually just cling to the bark in any way possible.
enclosed in the calyx area. On the foliage, mealy- Mealybugs of the Phenacoccus type may also be
bugs such as Planococcus citri (Risso), found encysted in the centre of the trunk of the
Pseudococcus longispinus (Targioni-Tozzetti) perennial plant itself. Perhaps these pseudococ-
and P. obscures Essig are common. cids gain entrance into this area through cracks in
Stems and twigs of perennials are also good the bark, but they appear to be completely
areas for mealybug colonies. Normally, the enclosed by the plant tissue. Phenacoccus arte-
mealybugs are found wedged into the cracks and misiae Ehrhorn is an example of this type of
crevices of the bark, again showing a preference mealybug.
for tight areas. Stems and twigs of plants are not Very often, the plant parts, both above and
nearly as important as roots, crowns and leaf below the ground, are utilized by certain boring
axils, but mealybugs such as Spilococcus eriogoni insect larvae. Commonly, if these boring tunnels
(Ehrhorn), Phenacoccus delectus Ferris and P. are pulled open, heavy infestations of certain spe-
alleni McKenzie are occasionally found restricted cies of mealybugs will be discovered.
to the branches. Most often, branches are an Phenacoccus eremicus Ferris seems to depend
overow area from the heavily infested leaf axils. upon the cerambycid boring tunnels for its total
The habitat of the mealybugs may be divided existence during detrimental weather. When
into two parts: the part which is above the ground snow is on the ground or temperatures are consis-
(arboreal) and that which is below the ground tently above 100 F, these mealybugs are found
(hypogeal). Very heavy infestations often occur only in the cerambycid tunnels. Apparently, the
below the ground. Frequently, this area becomes tunnels are an ideal setting for this pseudococcid,
so heavily contaminated with mealybugs that for the empty cavities surrounding the beetle
they often overow onto the roots. It should be larva are quite often completely full of mealy-
noted that only very rarely does this overow of bugs in all stages of development. During more
soil-inhabiting mealybugs move to the plant parts favourable weather conditions, infestations out-
above the soil surface. Many species of mealy- side of the tunnels are quite common.
bugs are entirely restricted to the root region.
These mealybugs can be divided into two types:
those that inhabit the main, large roots, and those 12.2.2 Annual Flowering Plants
that restrict themselves to the small eshy roots.
Cracks and crevices are the common areas of Mealybugs infesting annual plants are unique in
infestation on the main roots, but on the eshy that their host is present for only a small part of
roots, infestations may occur in any area where the year. The location of these mealybugs during
there is a vacant space. Species commonly col- that part of the year when their host plant is
lected in the large root areas are Phenacoccus absent is still a question. This is still a mystery.
solani Ferris, P. artemisiae Ehrhorn, For example, a very heavy infestation of
Chorizococcus polyporus McKenzie, Puto paci- Phenacoccus eschscholtziae McKenzie was
cus McKenzie, Chnaurococcus trifolii (Forbes) found in early April on a large variety of annual
and many more. Species found in the second hosts. But no mealybugs were found on plant
group are usually representatives of the genus parts either above or below the ground after 2
Rhizoecus, with R. falcifer Kunckel d'Herculais, months. Probably the annual-infesting mealy-
R. gracilis McKenzie and R. kondonis Kuwana as bugs, the disappearance of the pseudococcid with
good examples. its host, are still a mystery. Infestations on annual
Infestations of moderate- to small-sized hosts are localized in the subterranean areas, and
mealybugs usually occur in cracks and crevices there are mealybugs that are commonly found on
on the bark, whereas large species such as Puto the foliage of such hosts.
12 Ecology 143

12.2.3 Grasses roots or the foliage of the conifer are the areas of
early development and the bark is merely a rest-
Mealybugs are found on grasses in three areas: ing place for later development where no feeding
the foliage, crowns and roots. Most of the mealy- occurs. In the case of Puto sandini Washburn,
bugs inhabit the leaf-blade sheath of the grass which infests Engelmann spruce, Picea engel-
plant. This type of pseudococcid is especially mannii, in Utah, at elevations of 10,00011,200
adapted to its habitat in that it is dorsoventrally ft, this mealybug goes through a very compli-
attened, allowing it to t comfortably in its cated 4-year life cycle involving annual multiple
sheath environment. Trionymus is the most com- migrations. As a demonstration of the complexity
mon genus of this type, with T. dolus Ferris, T. of the life cycle, here is what happens during the
smithii (Essig) and T. festucae (Kuwana) being rst year. The mature adult females produce the
good examples. Mealybugs are found on the leaf rst-instar nymphs under the bark chips on the
surfaces of the Gramineae. Again, Trionymus is a bole of the tree. These nymphs migrate from the
good example of this type of infestation. Some bole to the duff at the base of the tree in late
mealybugs are found in the crown regions of September where they remain under the snow
Gramineae, for example, Discococcus spp. Some until sometime in May. At this time, they migrate
mealybugs are found at the nodes of the grass back up the tree to the foliage where they feed
stems, for example, Antonina graminis (Maskell). until mid-July. At this time, they migrate back
Some of these mealybugs feed on the tender ter- down the bole and hide in the bark crevices. In
minal roots of the grass, where they are exposed September, many specimens go back to the foli-
to the surrounding soil with little or no waxy pro- age again where they feed intermittently until late
tection. Cryptoripersia, on the other hand, occurs September. They then move down to the ground,
in the same area on the roots, but is covered by a crawl into the duff where they remain until the
tough, felted sac. Another root area is inhabited following May. This type of migration seems fea-
by Discococcus spectabilis McKenzie. The sible for other conifer-infesting Puto because in
mature adult females of this mealybug form their some California species there are known records
ovisac at the base of the plant just a few millime- of infestations in the duff, on the bark and in the
tres below where the roots were rst produced foliage.
from the culm base. Areas other than the bark of conifers are also
infested. The foliage region is particularly well
inhabited. In most instances, the mealybugs are
12.2.4 Conifers found at the bases of the needles. As far as is
known, the total life cycle of these species is
The genus Puto contains several species which spent in the region of the foliage. Some species
inhabit various types of conifers. Most of them found in the foliage area are Crisicoccus pini
have been found only in the cracks in the bark or (Kuwana), Dysmicoccus pinicolus McKenzie, D.
under the rocks and fallen logs. This host posi- ryani (Coquillett), Ehrhornia cupressi (Ehrhorn),
tion is quite extraordinary because it would seem Puto cupressi (Coleman) and Spilcoccus implica-
virtually impossible for the mealybugs to gain tus Ferris. Root infestations in coniferous trees
any nourishment from such inanimate objects. are not common.
Some of these pseudococcids have been found on Fern-inhabiting mealybugs are not at all
the bark at the base of the trunks of redwood trees common. Rhizoecus pritchardi McKenzie is,
well over 150 ft tall. The bark in this area would however, a species which is often found on
undoubtedly be over ten times thicker than the the roots of maidenhair fern, and is perhaps
length of the mealybug stylets. more commonly associated with the roots of
Perhaps these late-instar nymphs were able to African violet. Several other mealybugs are
sustain themselves completely on nutrients gath- also found on, although not restricted to, vari-
ered in the early parts of their life history. The ous types of ferns in nurseries. Perhaps the
144 M. Mani and C. Shivaraju

most common species in this category is cially temperature and relative humidity (RH),
Pseudococcus longispinus (Targioni- are major ecological factors that have been found
Tozzetti). Several species of Pedronia are to severely affect mealybugs and their natural
restricted to ferns in Hawaii. enemies.

12.2.5 Inanimate Objects 12.4.1 Overwintering

Occasionally, mealybugs are found in association Temperature is the driving force for mealybug
with nonbiological objects, especially during development. Many mealybugs overwinter as
winter. Misericoccus arenarius (Done and second-instar nymphs, although adult females,
Steinweden) is often found under the rocks or rst-instar nymphs and eggs also can full this
cracks in the rocks during the winter period. function (Miller 2005). For example,
Phenacoccus colemani Ehrhorn is commonly Phenacoccus azaleae Kuwana overwinters as a
found in the pits and crevices under the lava rocks. second-instar nymph within a wax cocoon (Xie
Heliococcus stachyos (Ehrhorn) is found under et al. 1999), Planococcus vovae as rst and sec-
the rocks deeply embedded in cracks in the rocks. ond instars (Francardi and Covassi 1992),
Wooden boards also serve as the habitat of some Pseudococcus viburni as rst instar in bark crev-
mealybugs. Chorizococcus rostellum (Hoke) is ices, and rarely as second or third instars
commonly found under the wooden boards. (Kosztarab 1996), and Pseudococcus maritimus
(Ehrhorn) as eggs and rst instar under the bark
(Geiger and Daane 2001). Ps. maritimus and Pl.
12.3 Host Plant Position cus overwinter primarily under the bark of the
trunk and cordon, with some of the population
Mealybugs show preference to certain positions found underground on the roots.
within the plant. Development of mealybug pop- The temperature has an impact on the devel-
ulation can be related to the plant growth and opment times and temperature thresholds for dif-
development. The mealybugs are relatively abun- ferent species. The number of generations of the
dant more on the fruits than on the other plant mealybug varies with the species, locality and
parts. This is true in several fruit crops. Mealybugs climatic factors. Most mealybug species are uni-
are found under loose bark and also on aerial or bivoltine, although some are reported to have
roots in the case of grapevine when fruit bunches as many as eight generations per annum in green-
are not available. Congregation of mealybugs is houses. There are ten generations of Planococcus
observed in the nodal region of the stem. They minor in a year, eight during FebruaryNovember
are seen usually on the lower surface of the and two during NovemberJanuary; M. hirsutus
leaves, more near the veins in the leaf. Mealybugs had ten generations per year in India. For exam-
are seen in large numbers on the fruits and are ple, Pseudococcus maritimus will have two gen-
rarely seen on the leaves and trunk in the case of erations in Californias interior valleys, whereas
custard apple. In ornamentals, the mealybugs are Planococcus cus can have seven generations in
distributed on the leaves, terminal shoots and the same region but is reported to have only three
ower buds. Some arboreal mealybugs extend generations per year in Italy. Similarly, Pl. citri in
their feeding on the parts just below the soil. Brazil has six generations per year in the south,
but up to 11 per year in the northeast where
grapes are produced throughout the year (two
12.4 Seasonal Development harvests per season). Other than Ps. maritimus
and H. bohemicus, there does not appear to be
Abiotic and biotic factors play a major role in the winter dormancy for the mealybugs. There is also
seasonal development of mealybugs besides the a variation in the seasonal feeding location and
phenology of the crop. Weather conditions, espe- movement on the plant among and within spe-
12 Ecology 145

cies, depending on factors such as regional tem- were registered at intervals of 2 h for 24 h on two
peratures and vineyard management practices, as separate days in July and September, respec-
described for Ps. maritimus and Pl. cus. The tively. In both the months, there was a high peak
mealybug population overwinters primarily of activity at sunset and a lower one at sunrise; in
under the bark of the trunk and cordon, with July, the peaks were separated by many hours of
some of the population found underground on the low catches, whereas in September the morning
roots, especially when tended by ants. There is no peak was much higher and the morning and eve-
diapause. On warm days, development may occur ning peaks were somewhat closer together than
during the winter months, with completion of the in July, owing to the shorter day length.
rst generation almost entirely under the bark. In tropical countries, the mealybugs occur on
From spring to summer, the Pl. cus population the plants throughout the year. Development of
follows the movement of plant resources from mealybug population can be related to the plant
roots to shoots to leaves. Four to ve generations growth and development. The mealybugs will be
are completed and population density can relatively abundant more on the fruits than on the
increase rapidly, although high summer tempera- other plant parts. The population is low in winter
tures, in excess of 40 C, may slow the growth of and rainy seasons and higher in summer months.
the population and increase mortality. As berries There was a highly signicant positive correla-
ripen and sugars develop, mealybugs move into tion of maximum and minimum temperature and
the berry clusters, rst attacking those near the a highly signicant negative correlation of morn-
vine cordon. The rapid population increase in ing and evening relative humidity and a nonsig-
summer is followed by an equally rapid decline nicant negative correlation of rainfall with
after harvest, resulting from biological controls mealybug population in vineyards in South India.
and abiotic mortality associated with high tem- They manage to survive under loose bark, feed-
peratures and vine senescence. ing at bases of spurs and callus tissue at the site of
The optimal temperature for populations of girdles in the off-season. In the absence of rains,
the cassava mealybug is between 20 and 30 there is a sudden spurt in the mealybug popula-
C. The cassava mealybug has poor survivability tion in dry seasons. Females of the mealybug
during rainy season because it is washed off the Glycycnyza turangicola are enclosed in a capsule
plant and drowns. The preferred temperature formed by hardened honeydew. This specializa-
range for the vineyard mealybug Planococcus tion is regarded as an adaptation to desert condi-
vitis (Nied.) was 1634 C, and this preference tions where humidity is extremely low in the
was unaffected by relative humidity. Linear Amudarya plain.
velocity increased with rises in the temperature. Heavy sporadic rains and cool temperatures of
Individuals that had been preconditioned at 95 % less than 20 C result in the temporary reduction
RH showed no consistent preference when pro- in the mealybug population. The pest population
vided with a choice of relative humidities, but build-up coincides with a high temperature of
those that had been desiccated avoided low 3040 C, low humidity (less than 40 %) and
humidities. The degree of humidity is probably fruit development.
perceived over the whole body. The mealybug is There is also a variation in the seasonal feed-
photonegative, and the reduced compound eyes ing location and movement on the vine among
are probably the photoreceptors. A rough sub- species and within species depending on regional
stratum was generally preferred to a smooth one. temperatures and vineyard management
Temperature appeared to be the main factor practices. There is no diapause, and slow devel-
determining the behaviour of the adults, and ori- opment may occur during the winter months
entation in relation to temperature, light, humid- under South Indian conditions. M. hirsutus was
ity and contact is mainly achieved by klinokinesis, active during winter also, without hibernation but
klinotaxis and orthokinesis. Catches of the male was most active during MarchOctober on roselle
mealybug, Pseudococcus calceolariae (Mask.), around West Bengal. In North India, the mealy-
146 M. Mani and C. Shivaraju

bug M. hirsutus on mesta overwintered in over- The ensete root mealybug Cataenococcus
lapping stages in the capsules of mesta beneath ensete Williams and Matile-Ferrero is a major
the persistent calyx and epicalyx of the old and pest in the ensete-growing regions of southern
dried plants and also in the soil during December Ethiopia. The ensete root mealybug, was
and January, when food plants were not avail- observed between 1054 and 2977 meter above
able. Mealybugs developed from a fraction of sea level (masl). Its infestation was severe only
third-generation eggs that did not enter winter between 1400 and 2200 masl. The highest infes-
diapause. tation (53.6 %) was recorded between 1600 and
Water-stressed plants have been reported to 1800 masl (Addis et al. 2010).
favour the increase in the mealybug population.
High nitrogen application enhances the results in
increase in the population of mealybugs. 12.4.2 Dispersal
In Java, Ferrisia virgata appears in large num-
bers during dry seasons of the year. It is more Adult male mealybugs are winged. The rst-
abundant from February to May in Philippines. instar nymphs (crawlers) have been found to
In Saudi Arabia, three generations were observed possess numerous characteristics that have been
in a year, early June, early July and August, and considered adaptations for dispersal behaviour,
the population increased with each generation. It including long legs and antennae (Gullan and
overwintered between January and early June as Kosztarab 1997). Adult males and newly
an adult female in the cracks and crevices of emerged rst-instar nymphs of most mealybug
trunks and branches and also on the fallen leaves. species display dispersal actively. Most mealy-
The female mealybug also migrated to the soil in bugs remain relatively stationary throughout
winter. The peak activity of F. virgata was their life (Miller 2005). However, some species
observed during JuneSeptember in West Bengal. move to different areas of the host for overwin-
On a number of host plants, it was most active tering, feeding, mating, ovipositing and moult-
during AugustNovember and MarchApril but ing (Franco 1994; McKenzie 1967; Miller 2005).
was very much reduced during December The occurrence of seasonal movements within
January (Mani and Krishnamoorthy 1993). the host has been reported for various mealybug
Several environmental factors inuence the pop- species, especially those associated with woody
ulation of F. virgata. Numerous records refer to plants such as Pl. citri, Ps. calceolariae, Ps.
heavy attack by F. virgata after prolonged viburni and Ps. longispinus in citrus (Franco
drought. The mealybug is favoured by dry 1994; Nestel et al. 1995); Pl. cus and Ps. mari-
weather in Java. The most important factor was timus in grapevine (Geiger and Daane 2001;
atmospheric humidity which exercises an indi- Godfrey et al. 2003); Pl. vovae in Juniperus spp.
rect effect through its inuence on parasitic fungi. (Francardi and Covassi 1992) and Ph. azaleae in
Temperature did not appear to have much effect bunge prickly ash (Xie et al. 1999). Franco
on F. virgata in Java. But a signicant positive (1994) suggested that immature feeding stages
correlation was found between the population of mealybugs on citrus tend to search for and to
density and daily maximum and minimum tem- settle at the major sinks, for example, growing
peratures in Saudi Arabia. Wind inuences the fruits, of the host plant in each phenological
dispersal and establishment of F. virgata in addi- period. We believe this hypothesis may also
tion by walking of the mealybugs. Windy areas explain the migratory movements of other
are highly susceptible to attack which is more mealybug species within various hosts. For
severe on hill tops than in valleys. F. virgata example, Pl. kraunhiae Kuwana was reported to
attacks the weak plants easily and spreads quickly feed on bacterium galls because they are sinks
on the younger plants exposed to sun and pro- for assimilates and have more nutritious phloem
tected from wind. It appears to prefer below sap and parenchyma than do normal plant tissues
5,000 ft altitude. (Yamazaki and Sugiura 2005). Other nymphal
12 Ecology 147

stages and adult female mealybugs are wingless, wild animals may aid the passive dispersal of
and some even legless; hence, they are not highly mealybugs (Kosztarab and Kozr 1988).
vagile, often xed to plants by their mouthparts Transport of nursery plants (ornamentals and
and always have a restricted distribution. fruit plants) infested with mealybugs aids the
However, the cassava mealybug (Phenacoccus spread of mealybugs from one location to
manihoti), rst reported in 1973 from the Congo another location.
areas of Kinshasa and Brazzaville, had become Among arthropods, ants have also been
established throughout the whole cassava belt of reported to disperse many mealybug species
Africa as far south as Mozambique by 1986 on (Gullan and Kosztarab 1997; Malsch et al. 2001;
the single plant genus Manihot (Herren and Ranjan 2006). Ants transported mealybugs from
Neuenschwander 1991). Mealybugs, particu- plant to plant between and within elds, thus
larly crawlers, having legs move limited dis- facilitating mealybug dispersal; adult females
tances within the plant and also between the and immatures of some mealybug species, asso-
plants (Kosztarab and Kozr 1988). Nevertheless, ciated with the ant genus Acropyga Roger, are
if conditions are favourable, crawlers usually carried by queens in their mandibles when found-
settle on the natal host plant, often close to their ing new colonies (Williams 1998). Associations
mother, which leads to an aggregative distribu- among invasive species of ants and mealybugs
tion (Gullan and Kosztarab 1997; Nestel et al. can be important in their success in new locations
1995). Similarly to most scale insects, crawlers (Helms and Vinson 2002). It is also observed that
are the mealybugs main dispersal agents, even mealybugs and other scale insects cling to locusts
though the mortality is very high (Gullan and during swarming. Misra (1920) reported another
Kosztarab 1997). First-instar mealybugs are eas- phoretic method of eggs and nymphs of
ily transported by the wind (Gullan and Maconellicoccus hirsutus (Green) being trans-
Kosztarab 1997). However, Williams and ported by nymphs and adult females of another
Granara de Willink (1992) reported that mealy- mealybug Ferrisia virgata (Cockerell).
bugs were believed to be distributed by air cur- All these methods are responsible for the local
rents over only short distances. In addition, and short-distance dispersal. Long-range disper-
dispersal strategies may be more passive, and sal of mealybugs is usually accomplished by the
crawlers of several species have been found to transport of infested plant material. Many species
exhibit behaviours that increase the chances of of mealybugs have been widely distributed by
wind dispersal and to use wind dispersal to commercial trafc, mostly carried on imported
migrate for several kilometres (Washburn and plant material (Williams and Granara de Willink
Washburn 1984). In India, Paracoccus margin- 1992). Papaya mealybug Paracoccus marginatus
atus spread very fast by wind dispersal of crawl- had spread very fast through the transport of
ers from the state Tamil Nadu to other states. fruits infested with mealybugs from Tamil Nadu
Crawlers from several species have also been to other states in India. Plants and their associ-
found to be able to survive without food for ated insects must have been carried to new areas
extended periods, which should again enhance by people for many centuries and people still
their dispersal success (Gullan and Kosztarab carry infested plant material, as shown by the
1997). Male and female nymphs do not differ in numerous quarantine interception records.
their dispersal behaviour or in their dispersal Because of their cryptic habits and small size,
success when dispersal is via crawler locomo- mealybugs are difcult to detect at borders dur-
tion. All the mealybug instars can be transported ing quarantine inspections, especially if their
on infested leaves blown by the wind. In addi- population density on plants is low (Gullan and
tion, water, bed-soil, humans and domestic and Martin 2003).
148 M. Mani and C. Shivaraju

References Kosztarab M, Kozr F (1988) Scale insects of Central

Europe. Dr. W. Junk Publishers, Dordrecht
Malsch AKF, Kaufmann E, Heckroth HP, Williams DJ,
Addis T, Azerefegne F, Alemu T, Lemawork S, Tadesse E,
Maryati M, Maschwitz U (2001) Continuous transfer
Gemu M, Blomme G (2010) Biology, geographical
of subterranean mealybugs (Hemiptera,
distribution, prevention and control of enset root
Pseudococcidae) by Pseudolasius spp. (Hymenoptera,
mealybug, Cataenococcus ensete (Homoptera:
Formicidae) during colony ssion? Inst Soc
Pseudococcidae) in Ethiopia. (Special Issue: Bananas,
Plantains and ensete II.). Tree For Sci Biotechnol
Mani M, Krishnamoorthy A (1993) Bionomics and man-
agement of the striped mealybug, Ferrisia virgata
Francardi V, Covassi M (1992) Biological and ecological
(CklI.) a review. Agric Rev 14(1):2243
notes on Planococcus vovae (Nasonov) (Homoptera,
Mckenzie HM (1967) Ecology in mealybugs of California.
Pseudococcidae) living on Juniperus spp. in Tuscany.
University of California Press, Berkeley, pp 1622
Redia 75:120 (in Italian, English abstract)
Miller DR (2005) Selected scale insect groups (Hemiptera:
Franco JC (1994) Citrus phenology as a basis to study the
Coccoidea) in the southern region of the United States.
population dynamics of the citrus mealybug complex
Fla Entomol 88:482501
in Portugal. In: Tribulato E, Gentile A, Reforgiato G
Misra CS (1920) Tukra disease of mulberry. Report of the
(eds) Proceedings of the international society of citri-
proceedings of the third entomological meeting held at
culture, Acireale, Italy, 1992. International Society of
Pusa on 3rd to 5th February 1919, pp 610618
Citriculture 3:929930
Nestel D, Cohen H, Saphir N, Klein M, Mendel Z (1995)
Geiger CA, Daane KM (2001) Seasonal movement and
Spatial distribution of scale insects comparative
distribution of the grape mealybug (Homoptera:
study using Taylors power-law. Environ Entomol
Pseudococcidae): developing a sampling program for
San Joaquin Valley vineyards. J Econ Entomol
Ranjan R (2006) Economic impacts of pink hibiscus
mealybug in Florida and the United States. Stochast
Godfrey K, Ball J, Gonzalez D, Reeves E (2003)
Environ Res Risk Assess 20:353362
Biology of the vine mealybug in vineyards in the
Washburn JO, Washburn L (1984) Active aerial dispersal
Coachella Valley, California. Southwest Entomol
of minute wingless arthropods: exploitation of bound-
ary layer velocity gradients. Science 223:10881089
Gullan PJ, Kosztarab M (1997) Adaptations in scale
Williams DJ (1998) Mealybugs of the genera
insects. Annu Rev Entomol 42:2350
Eumyrmococcus Silvestri and Xenococcus Silvestri
Gullan P, Martin JH (2003) Sternorrhyncha (jumping
associated with the ant genus Acropyga Roger and a
plant lice, whiteies, aphids, and scale insects). In:
revision of the subfamily Rhizicinae (Hemiptera;
Resh VH, Card RT (eds) Encyclopedia of insects.
Coccodea, Pseudococcidae). Bull Nat Hist Mus Lond
Academic, Amsterdam
Entomol 67:164
Helms KR, Vinson SB (2002) Widespread association of
Williams DJ, Granara de Willink MC (1992) Mealybugs
the invasive ant Solenopsis invicta with an invasive
of Central and South America. CABI, Wallingford,
mealybug. Ecology 83:24252438
635 p
Herren HR, Neuenschwander P (1991) Biological control
Xie Y, Zhao J, Guo Y, Li Y, Zhang H, Guo Y (1999) The
of cassava pests in Africa. Annu Rev Entomol
biology of Phenacoccus azalea Kuwana, a pest of
bungle prickly ash (Zanthoxylum bungeanum Maxim)
Kosztarab M (1996) Scale insects of northeastern North
forest in northern China. Entomology 33:377382
America: identication, biology and distribution.
Yamazaki K, Sugiura S (2005) Hemiptera as cecido-
Virginia Museum of Natural History, Martinsville
phages. Entomol News 116:121126
Natural Enemies of Mealybugs
A.N. Shylesha and M. Mani

Mealybugs are found attacked by various natural Syrphidae, Cecidomyiidae, Chamaeyiidae and
enemies in nature. The outbreak of mealybugs Drosophilidae (Diptera) are known to feed on
was observed in many instances with the applica- the mealybugs besides the spiders, mantids,
tion of broad-spectrum insecticides, which might ground beetles, assassin bugs, predatory stink
have disturbed the activity of natural enemies bugs, minute pirate bugs and predatory thrips.
particularly parasitoids and predators. This They are polyphagus feeding on a variety of
clearly indicates the importance of natural ene- mealybugs. Naturally occurring predators are
mies in the regulatory role of the mealybug popu- capable of suppressing the mealybugs on several
lation. In fact, there is a very rich natural complex occasions.
on arboreal mealybugs, but there is a poor natural
enemy complex, particularly natural predators or
parasites on root mealybugs. Withdrawal of 13.1.1 Coleoptera
insecticides results in the reappearance of natural
enemies, thereby regulating the mealybug popu- Coccinellidae
lation. The natural enemies of the pests can be Both adults and larvae feed voraciously on all
divided into three categories depending on how stages of the mealybugs including the egg masses.
they feed on the pests. They are predators, para- The larvae of many predatory coccinellids are
sitoids or pathogens. covered with white waxy laments very similar
to the mealybugs. The adults are brightly
coloured. The eggs are oval shaped, yellow and
13.1 Predators very small. The larvae are voracious feeders
though the adults are also known to feed on the
Insects belonging to Coccinellidae (Coleoptera), mealybugs. Development from egg to adult bee-
Chrysopidae and Hemerobiidae (Neuroptera), tle takes 2530 days at 25 C. The species belong-
Lycaenidae and Noctuidae (Lepidoptera) and ing to genera Cryptolaemus, Brumus,
Aspidimerus, Stictobura, Orcus, Diomus, Nephus,
Sidis, Parasidis, Pseudoscymnus, Hyperaspis,
A.N. Shylesha (*)
ICAR-National Bureau of Agriculturally Important Scymnus, Sasajiscymnus, Exochomus,
Insect Resources, Bangalore 560 024, India Brumoides, Cleophora, Harmonia etc. are some
e-mail: of the important predators of mealybugs. Among
M. Mani the coccinellids, Cryptolaemus montrouzieri
Indian Institute of Horticultural Research, Mulsant was extensively used to control a variety
Bangalore 560089, India
of mealybugs throughout the world.

Springer India 2016 149

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_13
150 A.N. Shylesha and M. Mani

Cryptolaemus montrouzieri about 30 days at a temperature of 25 C. During

Cryptolaemus montrouzieri is native of Australia her lifespan, a female can lay up to 400 eggs.
popularly known as the Australian ladybird bee- The eggs are deposited within the egg masses of
tle, often referred to as the mealybug destroyer. the mealybugs. Cryptolaemus eggs are brighter
Adult beetles are about 4 mm long, oval in shape, and quite larger. The larvae are covered with
black in colour with a light brown head and pos- long white wax laments. At rst sight, they
terior. Cryptolaemus larvae grow up to 13 mm very closely resemble the mealybugs. However,
long and are covered with long, white, waxy la- Cryptolaemus larvae move faster and are more
ments. The Cryptolaemus preys upon several uffy in their appearance. The larvae will eat
species of mealybugs. It is less effective when each other whenever the food availability is poor.
the temperature is below 20 C or when the For pupation, the larvae will go to a hidden
humidity level is low (<40 % relative humidity place. The pupae look very similar to the larvae,
(RH)). Cryptolaemus prefers a warm and humid quite larger and somewhat more uffy (Mani
climate. The egg to adult development takes et al. 1991).

Cryptolaemus on mealybugs Nephus includens

Hyperaspis trilineata Mulsant can, during her lifetime, lay from 300 to 400
Hyperaspis trilineata Mulsant is a principal pred- eggs. The larvae are covered with white waxy
ator of Saccharicoccus sacchari (Cockerell). It is laments, very similar to that of mealybugs. The
reported to have a peculiar type of egg that is at beetle larvae are ufer and can run faster. The
rst at and resembles a whitey larva. They are larvae are often little in the crop because they are
laid singly and are hatched in 810 days. The very small and often found in the egg mass of the
young larvae feed for a time on mealybug crawl- mealybug. The eggs of mealybugs are oval
ers before developing their cottony covering. shaped, yellow and very small, but in practice not
About 3 weeks are required for larval develop- visible. Both adult beetles and larvae eat mealy-
ment followed by pupal development and adult bugs. When a mealybug is eaten, the dead
emergence. remains can be seen on trees as white uffy mat-
ter. The larvae mainly feed on eggs and young
Nephus includens Kirsch mealybugs. They can consume up to about 100
Nephus includens Kirsch is a predator of the cit- eggs per day or about 50 young mealybugs.
rus mealybug. Adult beetles are dark; they have
four orange/yellow spots on their backs. They are Scymnus coccivora Ayyar
about 2 mm in size. Its eggs are laid in the egg Scymnus coccivora Ayyar is known to feed on
mass laid by the mealybug. The female beetle several species of the mealybugs. Adults are light
13 Natural Enemies of Mealybugs 151

brown in colour measuring 1.7 1.3 mm in size. 1.2 and 5.2 days, respectively, and the total life
The pale yellow eggs are deposited singly in the cycle is completed in 23 days. The sex ratio is
colony of mealybugs. The grub has instars. Long 1:1. A single grub S. coccivora was known to
waxy strands develop on the later stage of the consume 308 eggs or 62 nymphs or 6.55 adult
grub. The pupa is oval and light brown in colour mealybugs (Mani and Thontadaraya 1987).
fringed with short brown hairs. The egg, grub,
prepupal and pupal stages occupy 4.1, 4.2, 9.5,

C. sexmaculata B. suturalis H. octomaculata Nephus regularis S. coccivora

13.1.2 Neuroptera length, usually on the underside of a leaf.

Immediately after hatching, the larvae moult, Chrysopidae then ascend the egg stalk to feed. The larvae are
Green lacewings are delicate insects 14- to 12- spindle shaped, some camouaged within the
in. long with a wingspan of 6 to >65 mm, and the host mealybugs. They are voracious predators.
largest forms are tropical. Adults are often seen Larvae of green lacewings found feeding the
around the foliage. They are characterized by a early stage of mealybug nymphs. A single larva
wide costal wing venation, which includes the of Mallada boninensis is capable of consuming
cross veins. The bodies are usually bright green 350500 nymphs in its development. The spe-
to greenish-brown, and the compound eyes are cies belonging to genera Chrysopa, Chrysoperla
conspicuously golden in many species. The and Mallada are the well-known predators of
wings are usually translucent with a slight irides- mealybugs. The stalked eggs of the green lace-
cence; some have green wing veins or a cloudy wings are commonly seen in many plants
brownish wing pattern. Eggs are deposited at infested with sucking pests including mealy-
night, singly or in small groups; each female bugs. Chrysoperla carnea is used to control the
produces approximately 100200 eggs. Each mealybugs in green houses. They carry the trash
egg is hung on a slender stalk about 1 cm in over their bodies.

Life stages of green lacewing

Adult Eggs Larva on mealybugs Larva carrying trash

152 A.N. Shylesha and M. Mani

Mallada boninensis veins are forked. The larvae of the brown lace-
A single larva of M. boninensis was able to prey wings belonging to genus Hemerobius, and
about 345, 490 and 560 nymphs of Ferrisia vir- Sympherobius prefer to prey the early stage of the
gata, Planococcus lilacinus and P. citri, respec- mealybugs, though they are known to feed all the
tively (Mani and Krishnamoorthy 1990). three nymphal instars of the female mealybugs.
The rst-instar larvae of Sympherobius fallax
Chrysoperla carnea consume the second stage of the long-tailed
The larvae of the Ch. carnea grubs were found as mealybug P. longispinus more than any other
active predators on the mealybugs, and the preda- stages and did not eat the fourth (adult) stage,
tory grub preyed on all the stages of the mealy- while the second-stage S. fallax preferred the
bug. A single larva was known to consume 378 third-stage mealybugs. The third-stage S. fallax
eggs or 730 nymphs, or 95 adult females of P. also preferred the third-stage mealybugs. In the
citri. choice experiment, the rst-stage larval predators
preferred the second-stage mealybugs signi- Hemerobiidae cantly more than the other two stages, while the
Hemerobiidae is a family of the Neuropteran second- and third-stage predators preferred the
insects commonly known as brown lacewings. third-stage mealybugs signicantly more than the
These insects differ from the somewhat similar second and the fourth stages. Darkness had a
Chrysopidae (green lacewings) not only by the marked effect on the feeding efciency of all
usual colouring but also by the wing venation. stages of S. fallax. The number of mealybugs
Hemerobiids have numerous long veins that are eaten in the light was signicantly greater (Gillani
lacking in chrysopids. Some of the costal cross et al. 2009).

Larva of Sympherobius Adult Sympherobius

13.1.3 Lepidoptera same wing can be seen; in some specimens, this

spot is slightly diffused. On the underside, it is Lycaenidae pale, silky, brownish-white; fore- and hindwings
The Apey Spalgis epeus Westwood is a small crossed by numerous, very slender, short, sinu-
buttery found in Asia. It gets its name due to the ous, transverse, dark brown strigae, which are
face resemblance of ape that can be seen from the outwardly slender edged with brownish-white of
head-on view of the pupa. The male is dull brown a shade paler than that of the ground-colour. Both
on the upperside and slightly darker towards the the wings have an anticiliary dark brown line on
apex of the forewing; also a more or less quadrate the inner side with similar edging. Forewing, in
whitish spot beyond the apex of the cell on the addition, has an oval white spot beyond the cell.
13 Natural Enemies of Mealybugs 153

The cilia of both the fore- and hindwings are of slightly paler brown. In the forewing, the cell and
the same shade as that of the ground colour of the apex are darker, with a white spot similar to that
wings. The antenna, head, thorax and abdomen in the male but larger, beyond the apex of the cell;
are pale brown in colour, and the club of the in most specimens, it is extended diffusely out-
antennae is ochraceous at apex; beneath are the wards and downwards. The hindwing is similar
palpi and thorax brownish-grey and the abdomen to that of the male. The underside is as precise as
pale brown in colour. In female, the upperside is in the male.

Life stages of Spalgis epeus

Second instar caterpillar Third instar caterpillar Final instar caterpillar Adult buttery

The lycaenid predator Spalgis epeus was com- ing to Drosophilidae, Cecidomyiidae, Syrphidae
monly associated with the natural control of the etc. are known to attack the mealybugs. The
mealybugs Rastrococcus iceryoides, Planococcus dipteran larvae feed voraciously on the
lilacinus, Pl. citri, Ferrrisia virgata, Paracoccus mealybugs.
marginatus etc. The larvae of Spalgis epeus were
observed to predate on root mealybug colonies Cecidomyiidae
especially those at the base of the stems In this family, the larvae of a large number of spe-
(Devasahayam et al. 2009). Although Spalgis cies are predaceous on the mealybugs. These
lemolea was a common natural enemy of insects are very tiny, usually only 23 mm in
Phenacoccus madeirensis infesting cassava in length. The adults, which are very tiny, fragile
Africa (Herren and Neuenschwander 1991), its midges, locate colonies of appropriate prey. The
potential utility as an effective biological control eggs are laid near the base of the mealybug host;
agent was thwarted by its erratic occurrence. At the larva tunnel underneath the host and feed on
2530 C and 4060 % RH, the mean duration of the eggs or developing coccid nymphs. As the
the egg, larval and pupal stage of Spalgis epeus small, maggot-like larvae are incapable of mov-
on Pa. marginatus is 3.5, 12.0 and 10.3, respec- ing to considerable distances, there usually has to
tively, and the mean duration from egg to adult be a fair population of the prey present, before
emergence was 26 days, and it takes 24 days on the adults will lay eggs. The life cycle is com-
Pl. citri to complete the life cycle (Dinesh et al. pleted in 25 days. The total number of eggs
2010). As for the predatory potential of S. epeus, deposited by the female averaged 36 during her
the total number of papaya mealybugs consumed very short lifespan, which averaged 2.3 days. The
during the larval stage was 4,115 eggs, 281 larvae of Dicrodiplosis manihoti Harris were
nymphs and 77 female adults. found to prey on the egg masses of the cassava
mealybug, Phenacoccus manihoti in the Congo
and Senegal. Kalodiplosis pseudococci Felt has
13.1.4 Diptera given signicant control of D. brevipes in con-
junction with two parasitoids. Triommata coc-
Several dipterans are found as predators in the cidivora Felt plays a supplementary role in
concealed mealybug niche. The insects belong- regulating the mealybug population.
154 A.N. Shylesha and M. Mani Chamaeyiidae Syrphidae

Chamaeyiidae is a small family of acalyptratae Syrphid larvae are predatory on the mealybugs
ies. The larvae are the predators of the but are of minor importance (Table 13.1).
mealybugs. Drosophlidae 13.1.5 Other Predators

Larvae of the predatory drosophilids are found
feeding on the colonies of nymphs. They play a The rat Millardia meltada meltada gnawed
supplementary role in regulating the mealybug through the lower dry leaf sheaths and devoured
population. the mealybugs Saccharicoccus sacchari at the
nodes of sugarcane.

Pirate bugs feed on the mealybugs Crab spiders feed on the mealybugs

Table 13.1 List of predators recorded on the mealybugs

Predator species Mealybug species
Coleoptera, Coccinellidae Coccidohystrix insolita
Anegleis cardoni (Weise)
Brumoides suturalis (Fab.) M. hirsutus, P. lilacinus, F. virgata, Ph. solenopsis,
Pa. marginatus, Coccidohystrix insolita (Green)
Cryptolaemus montrouzieri Mulsant Many mealybug species
Coleophora pupillata (Schonherr) Several mealybugs
Cheilomenes sexmaculata (Fab.) Ph. soleneopsis, F. virgata, Pa. marginatus
Curinus coeruleus Mulsant Nipaecoccus nipae (Maskell)
Chilocorus stigma (Say) Pl. citri
Chilocorus nigrita (Fabricius) S. sacchari
Chilocorus sp. Pa. marginatus
Chilocorus bipustulatus L. Phenacoccus mespili Ben-Dov
Decadiomus bahamicus (Casey) Pl. citri
Diomus notescens (Blackburn) Several mealybugs
Diomus hennesseyi Fiirsch Ph. manihoti
Exochomus aviventris Mader Phenacoccus manihoti Matile-Ferrero
Exochomus troberti Mulsant Phenacoccus manihoti
Exochomus avipes (Thunberg) Phenacoccus manihoti
Exochomus concavus Fursch Phenacoccus manihoti
Exochomus metallicus Korsch Planaococcus citri (Risso)
13 Natural Enemies of Mealybugs 155

Table 13.1 (continued)

Predator species Mealybug species
Exochomus nigripennis (Erichs.) Nipaecoccus viridis (Newstead)
Exochomus melanocephalus (Zubkoff) Saccharicoccus sacchari (Cockerell)
Harmonia octomaculata (F.) Phenacoccus solenopsis Tinsley
Harmonia maindroni Sicard Maconellicoccus hirsutus (Green), P. lilacinus,
Coccidohystrix insolita (Green)
Hippodamia convergens (Gurin-Mneville) Ph. solenopsis
Hippodamia variegata Goeze Ph. solenopsis
Hyperaspis limbatus Casey Saccharicoccus sacchari (Ckll.)
Hyperaspis silvestri Weise Dysmicoccus brevipes (Cockerell)
Hyperaspis trilineata Mulsant Saccharicoccus sacchari
Hyperaspis onerata (Mulsant) Phenacoccus herreni Cox and Williams
Hyperaspis egregia Mader Planococcoides njalensis (Laing)
Hyperaspis marmottani (Fairm.) Phenacoccus manihoti
Hyperaspis senegalensis hottentotta Mulsant Phenacoccus manihoti
Hyperaspis raynevali (French) Phenacoccus manihoti
Hyperaspis aestimabilis Mader Phenacoccus manihoti
Hyperaspis pumila Muls. Phenacoccus manihoti
Hyperaspis onerata (Muls.) Phenacoccus manihoti
Horniolus vietnamicus Miyatake P. lilacinus
Midas pygmaeus Blackburn Ps. calceolariae
Nephus vetustus Weise Phenacoccus manihoti
Nephus regularis Sicard Ph. solenopsis, Coccidohystrix insolita
Nephus reunion (Fursch Pseudococcus sp.
Nephus bipunctatus (Kug.) N. viridis
Nephus bilucernarius Mulsant Nephus bilucernarius Mulsant
Pesudoscymnus pallidicollis (Mulsant) M. hirsutus
Platynaspis strictica philippenensis Korchefsky Planococcus kenyae (LePelley)
Pseudoscymnus pallidicollis (Mulsant) Pl. citri
Pullus pallidicollis (Mulsant) P. lilacinus, Pl. citri
Sasajiscymnus quinquepunctatus (Weise) Paracoccus marginatus Williams and Granara de
Scymnus binaevatus Mulsant Pseudococcus calceolariae (Maskell)
Scymnus coccivora Ayyar M. hirsutus, P. lilacinus, F. virgata, Ph. solenopsis,
Pa. marginatus
Scymnus nubilus Muls. M. hirsutus
Scymnus syriacus F. virgate
Scymnus gratiosus Wiese M. hirsutus
Scymnus severini Weise P. lilacinus
Scymnus margipaliens Muls. D. brevipes
Scymnus couturier G. Ph. manihoti
Scymnus sp. Geococcus citrinus Kuwana
Scymnus avifrons Blackburn Pl. citri
Scymnus (Pullus) uncinatus Sicard D. brevipes
Scymnus pictus Gorham D. brevipes
Coleoptera, Nitidulidae S. sacchari
Carpophilus marginellus Motsch
156 A.N. Shylesha and M. Mani

Table 13.1 (continued)

Predator species Mealybug species
Coleoptera, Lathridiidae M. hirsutus
Melanophthalma carinulata Motsch
Diptera, Cecidomyiidae Planococcus kenyae, Planococcoides njalensis
Coccodiplosis coffeae (Barnes) (Donald)
Coccodiplosis citri Barnes Phenacoccus manihoti
Cleodiplosis koebelei (Felt) D. brevipes
Diadiplosis koebelei (Koebele) Several mealybugs
Diadiplosis coccidivora (Felt) F. virgate
Dicrodiplosis manihoti Harr. Phenacoccus manihoti
Dicrodiplosis sp. Planococcus citri, P. lilacinus, N. viridis
Gitona sp. F. virgate
Kalodiplosis koebelei (Felt) Ps. calceolariae
Kalodiplosis pseudococci (Felt) D. brevipes
Kalodiplosis coccidarum (Felt) Ph. herreni
Lobodiplosis pseudococci Felt D. brevipes
Triommato coccidivora (Felt) P. lilacinus (Risso)
Vincentodiplosis pseudococci D. brevipes
Diptera, Chamaeyiidae R. iceryoides, P. lilacinus, Brevennia rehi
Leucopis luteicornis Malloch.
Leucopis sp. F. virgate
Leucopis ocellaris Mall Pseudococcus comstocki
Leucopis alticeps Czerny Phenacoccus mespili Ben-Dov, P. citri
Diptera, Drosophilidae P. citri, P. lilacinus, S. sacchari, Phenacoccus
Cacoxenus (Gitonides) perspicax (Knab) manihoti
Rhinoleucophenga capixabensis sp. nov. Dysmicoccus brevipes
Domomyza perspicax (Knab) P. citri, Brevennia rehi (Lindinger)
Diptera, Syrphidae
Ocyptamus argentinus Curr. F. virgata
Xanthogramma javana Wd. F. virgate
Allobaccha eclara (Curran) Phenacoccus manihoti
Diptera, Chloropidae Brevennia rehi (Lindinger)
Anatrichus pygmaeus Lamb
Neuroptera, Chrysopidae M. hirsutus
Apertochrysa sp.
Anisochrysa basalis Walker Pl. citri
Anisochrysa boninensis (Okaomota) Coccidohystrix insolita
Brinckochrysa scelestes Banks M. hirsutus
Ceratochrysa antica (Wlk.) Phenacoccus manihoti
Chrysopa ramburi Schneider Ps. Calceolariae
Chrysopa sp. Phenacoccus manihoti, N. viridis
Chrysoperla carnea (Stephans) P. citri, F. virgate
Chrysopa lacciperda (Kimmis) P. citri, Ph. solenopsis, Ph. mespili
Chrysoperla rulabris (Burmeister) Ps. longispinus (Targioni Tozzetti)
Chrysoperla zastrowi Sillemi (Esben-Petersen) Pa. marginatus
Chrysopa lateralis Guerin Pl. citri
13 Natural Enemies of Mealybugs 157

Table 13.1 (continued)

Predator species Mealybug species
Oligochrysa lutea (Wlk.) Ph. solenopsis
Mallada boninensis (Okamota) Many mealybugs
Plesiochrysa lacciperda (Kimmins), Pl. citri
Neuroptera, Hemerobiidae Ps. calceolariae
Sympherobius amicus Navas
Sympherobius barberi (Banks) Ps. longispinus, P. citri
Sympherobius pygamaeus (Rambur) M. hirsutus
Psectra iniqua (Hagen) Rastrococcus invadens Williams
Neuroptera, Coniopterygidae M. hirsutus
Conwentzia psociformis (Curtis)
Cryptoscenea australiensis (Enderlein) Pseudococcus viburni (Signoret)
Lepidoptera, Lycaenidae Planoccuus kenyae, F. virgata, P. manihoti
Spalgis lemolea Druce
Spalgis epeus West wood P. citri, P. lilacinus, Ph. solenopsis, Pa.
marginatus, Coccidohystrix insolita, Nipaecoccus
Lepidoptera, Pyralidae P. citri
Laetilia coccidivora (Comstock)
Lepidoptera, Momphidae S. sacchari
Batrachedra sp. near psilopa Meyrick
Lepidoptera, Noctuidae P. lilacinus
Eublemma sp.
E. geyri Rild M. hirsutus
E. trifasciata Moore M. hirsutus
Autoba silicula Swinhoe M. hirsutus
Hemiptera, Coreidae M. hirsutus
Geocoris tricolor (Fab.)
Hemiptera, Miridae F. virgate
Deraeocoris sp.
Hemiptera: Anthocoridae Ph. manihoti
Cardiastethus exiguus Poppius

13.2 Parasitoids Encyrtidae

Major parasitism in the mealybugs involves mem-
13.2.1 Hymenoptera bers of the wasp family Encyrtidae. The encyrtids
are koinobiont endoparasitoids, so that the parasit-
The parasitoids belonging to families Encyrtidae, ized mealybug continues to live for a few days, to
Aphelinidae, Platygastridae, Pteromalidae, grow and even to reproduce to some extent. This
Braconidae, Eucoilidae, Signiphoridae and time gap between parasitization and deterioration of
Eulopidae are known to attack the mealybugs. the physiological condition enables the mealybug to
Among them, encyrtids, aphelinids and platygas- confront the immature individual parasitoid by
trids play a major role in the regulation of encapsulation. The encapsulation is a common
mealybugs. immune defense mechanism that involves the for-
mation of a capsule around the parasitoid egg or
158 A.N. Shylesha and M. Mani

larva; it is usually composed of host blood cells and full-grown parasitoid emerges through an exit hole
the pigment melanin. The capsule may kill the para- at the distal part of the cocoon, leaving the lid
sitoid and thus prevent successful parasitism behind. Full development of the parasitoid takes
(Blumberg 1997). Various levels of encapsulation place inside the mealybug. Adult parasitoids feed
have been shown to occur in different mealybug themselves by piercing the young instars of the
species, in response to parasitism by encyrtids mealybugs and sucking from their bodies. By
(Blumberg 1997; Blumberg and van Driesche 2001; doing so, they can extend their lifespan. This feed-
Chong and Oetting 2007; Giordanengo and Nenon ing behaviour kills the young mealybug-instars.
1990; Sagarra et al. 2000). Conversely, encyrtid Parasitized mealybugs turn into a yellow/orange
parasitoids may use superparasitism as a strategy to cocoon and become hard (like mummies). These
overcome the immune response of unsuitable hosts mummies are difcult to see, because of their
(Blumberg et al. 2001). Besides superparasitism, small size. In this period, a female can lay about 80
other factors also affect the frequency of parasitoid eggs, most of them in the rst weeks of her life.
encapsulation including: (a) host and parasitoid spe- Anagyrus is a large genus of the family
cies; (b) the hosts physiological age and condition; Encyrtidae that attacks the mealybugs. Some
(c) the host and parasitoid origins (or strains); (d) important species like Anagyrus aegyptiacus, A.
the rearing and/or ambient temperature; and (e) the dactylopii, A. kamali, A. pseudococci play the
host plant species and stress conditions (Blumberg major role in suppressing the mealybugs. Other
1997; Calatayud et al. 2002). encyrtids, namely Leptomastidea abnormis,
Noyes and Hayat (1994) recorded 49 encyrtid Leptomastix dactylopii, Acerophagus papayae,
species as parasitoids of mealybugs in India. The Apoanagyrus lopezii, Aenasius bambawalei and
family Encyrtidae dominates the parasitoid com- Aenasius advena Comp., are found to be very
plex of mealybugs. Anagyrus, Apoanagyrus, effective parasitoids of mealybugs.
Adolescentus, Aenasius, Leptomastix,
Leptomastidea, Blepyrus, Gyranusoidea, Anagyrus antoninae (Timberlake)
Praleurocerus, Mahencyrtus, Acerophagus, It is an internal gregarious parasite of Antonina
Coccidoxenoides, Epidinocarsis, Neodusmetia, graminis. It is oriental in origin but common in
Hambletonia, Pseudaphycus and Alamella are Hawaii. It is active in cooler and high-humid areas.
some of the important genera under encyrtidae The female mates soon after the emergence and
attacking the mealybugs. They are sexually dimor- starts laying eggs immediately. Attack is on the
phic and both males and females are different from gravid female mealybugs. The stalked eggs are
each other. The males are smaller than the females unattached and free in the body uids of the mealy-
and have hairy antennae. The females have a bright bug and are hatched in 34 days. The larval and
band across the abdomen. The encyrtids are known prepupal stages cover 810 days. The pupal stage
to attack nymphs and adults of mealybugs. Each takes about 68 days, and the total life cycle is
species tends to specialize in terms of the stage of completed in 18 days. Up to seven adult parasites
development of the host. Certain species like emerge per mealybug and the sex ratio is 1:1. It is
Blepyrus insularis, Coccidoxenoides perminutus, carried out very well under Florida conditions.
Acerophagus papayae prefer earlier stage that is
58-day-old nymphs (early Second instar) for par- Neodusmetia sangwani (Subba Rao)
asitization, whereas species like Anagyrus dacty- It is an internal gregarious parasitoid of Antonina
lopii, Leptomastix dactylopii etc. prefer graminis and is native to India. Adult females are
1520-day-old mealybugs (third instar and young brachypterous and males are winged. They live
adult female). They breed very well when they are only for 2 days. The female produces up to 55
exposed to the preferred stage. The duration of the progeny. The sex ratio is 1:7. Life cycle is com-
life cycle is about 3 weeks at 25 C. Mealybugs pleted in 1723 days. Normal dispersal is very
that are parasitized turn into small cocoons, a little slow since the females are wingless. It has done
darker in colour than live mealybugs. The young very well under Texas conditions.
13 Natural Enemies of Mealybugs 159

Neodusmetia sangwani Hambletonia pseudococcina

Pseudaphycus mundus Gahan Blepyrus insularis

It is mainly a parasitoid of Dysmicoccus boni- It is also another internal parasitoid of F. virgata,
nensis, native of Lousiana. It attacks all stages of preferring to parasitize the early instars of the
the mealybug except the rst-instar nymphs. It mealybugs. It performs very well in glasshouse
deposits eggs in the body uids of the mealybug. crops infested with F. virgata (Mani and
From 2 to 15 min is required for oviposition. It Krishnamoorthy 1991).
takes 1618 days to complete the life cycle. It is
solitary in small mealybugs but lays up to 19 Coccidoxenoides perminutus
eggs on larger mealybugs. It did very well Coccidoxenoides perminutus Girault (Pauridia
against D. boninensis in sugarcane elds at peregrina Timberlake, Coccidoxenoides peregri-
Hawaii. nus (Timberlake)) is an endoparasitoid of
Planococccus citri widely present throughout the
Hambletonia pseudococcina Compere world. Coccidoxenoides perminutus alone or
It is bisexual in Brazil and unisexual in Columbia. along with other natural enemies is capable of sup-
The unisexual race was found to be relatively pressing P. citri. Besides Pl. citri, it also attacks
successful against D. brevipes in Hawaii. It is a Pseudococcus longispinus, Pl. cus and
solitary parasitoid. The females attack half- Pseudococcus viburni. Adult parasitoids are black
grown mealybugs and takes 2430 days to com- in colour with noticeable translucent wings, with
plete the life cycle. relatively long antennae and are approximately
3 mm long. Females lay their eggs into the rst
Aenasius advena three instars but prefer the second instar of Pl. citri
Aenasius advena Comp is a solitary internal par- and are able to lay 6090 eggs each. The eggs
asitoid of Ferrisia virgata. It occurs in large num- develop into pupae within the mealybug slowly
bers at times on F. virgata in guava and other crop feeding off the host. About 16 days after egg lay-
ecosystems in India and elsewhere. It prefers ing, adult C. perminutus wasps emerge from
15-day-old mealybugs and the lifecycle is com- pupae, and are immediately ready to mate and
pleted in about 18 days. Along with C. montrouz- continue the cycle. The speed of the lifecycle is
ieri, A. advena gives the perfect control of F. dependent on temperature and humidity. Generally,
virgata on guava and other crop ecosystems in C. perminutus adults are active for about 7 days
India. and are most effective at temperatures between 20
and 30 C and humidity between 50 and 90 %.
Each female lives for approximately 7 days.
160 A.N. Shylesha and M. Mani

Anagyrus fusciventris (Girault) bright blue eyes. Males are black in colour. Both
It is a parasitoid of Pseudococcus longispinus. sexes are about 3 mm in size. Mealybugs that are
Females are grey-brown in colour and have

Coccidoxenoides perminutus Anagyrus fusciventris

parasitized turn into small cocoons, a little darker rate of three to four per day. The eggs hatch in 44 h
in colour than the live mealybugs. It prefers larger and the lifecycle is completed in 18 days at 27 C.
instars for parasitization. The females lay one egg
per host; from each parasitized mealybug, one Leptomastix dactylopii Howard
adult wasp will emerge. The lower temperature It is widely used against Planococcus citri.
threshold for the parasitoid is 18 C. The parasit- Besides P. citri, it also breeds well on Pl. cus.
oid development from egg to adult takes about 3 It is a small yellow-/brown-coloured parasitic
weeks at a temperature of 25 C. Full development wasp with distinctively long dark antennae. It is
of the parasitoid takes place inside the mealybug. about 3 mm long. Males are smaller and darker
Adult parasitoids feed themselves by piercing the than females. The antennae of the females are
young instars of the mealybugs and sucking from bended; the antennae of the males are hairy. Eggs
their bodies. By doing so, they can extend their life are laid in the third instar and in the young adult
span to about 2 months. This feeding behaviour female mealybug. The females deposit one egg
kills the young mealybug instars. inside the mealybug body. A female lays about 100
eggs. After hatching, the young larva of the parasit-
Anagyrus pseudococci (Girault) oid eats the mealybug from inside out. The parasit-
Anagyrus pseudococci (Girault) is native of ized mealybugs turn into a yellow-brown cocoon
Mediterranean areas. It is known to attack Pl. citri and become hard (like mummies). The lower tem-
and Ps. citriculus. It attacks all the nymphal stages perature threshold for Leptomastix dactylopii is
and the adult females but prefers the third instar of the 20 C, but the optimal temperature is 26 C. At
mealybug. About 45 eggs are laid per female at the 25 C, this development takes about 1517 days.

Anagyrus pseudococci Leptomastix dactylopii

13 Natural Enemies of Mealybugs 161

Leptomastix epona The adult parasite emerges from a circular exit hole
It is a parasitoid of Pseudococcus viburni (Ps. af- at the proximal end of the cocoon, leaving a lid on
nis) and Spilococcus cactearum. Adult wasps are the mummy. It mainly parasitizes older instars of
brown-black with thin, long, black antennae. Their Ps. viburni and Spilococcus cactearum. It lays one
wings are mainly translucent with slight dark bands. egg per mealybug. Mealybugs are killed by the
Leptomastix epona is 3 mm in size. Mealybugs that growing larva approximately 10 days after parasit-
are parasitized turn into yellow cocoon like mum- ization. Lower temperature threshold for
mies, easily distinguishable from live mealybugs. Leptomastix epona is 15 C.

Leptomastix epona Pseudaphycus maculipennis

Acerophagus maculipennis Pseudaphycus malinus

Pseudaphycus maculipennis (Acerophagus mac- It is an internal parasitoid of Pseudococcus com-
ulipennis) was shown to be an arrhenotokous, stocki believed to be a native of Japan. It develops
synovigenic, gregarious endoparasitoid of as a solitary parasite in smaller mealybugs but
Pseudococcus viburni. Both females and males gregarious in larger mealybugs. Females deposit
lived for 16 and 11 days, respectively, when fed about 100 eggs in 410 days. Incubation is com-
either honey-agar or mealybug honeydew. pleted in 3 days, larval development in 8 days and
Relatively, large instars (third instar or adult pupal stage in 10 days.
females) were preferred for oviposition; mated
females parasitized more mealybugs than Leptomastidea abnormis
unmated females, and the progeny sex ratio Leptomastidea abnormis mainly parasitizes
favoured females by 3:1. Egg load increased with Planococcus citri. It is a grey-yellow parasitic
age from emergence to day 8, averaging 23 wasp, 0.751.5 mm in size; dark bands are clearly
mature eggs per female. Mean realized daily visible across the wings. Males are smaller than
fecundity never exceeded 5, with a mean lifetime females and have hairy antennae. The females
fecundity of 46 eggs per female. Parasitized have a bright band across the abdomen. The para-
mealybugs remained alive for about 5 days and sitized mealybugs turn into a yellow/orange
then mummied. Total development period was cocoon and become hard. Leptomastidea emerges
2021 days (larva 45 days, prepupa 3 days, from a circular hole in the proximal end of the
pupa 89 days). A mean of 3.0 parasitoids per mummy. Eggs are laid in the rst and second
mealybug were reared after individual parasitism instars of its host, one egg per mealybug. The
events, increasing through superparasitism inconspicuously stalked eggs are laid in the body
(either self or conspecic) to nine parasitoids per uid of the mealybugs and are hatched in 3 days.
mealybug when hosts were exposed to competing The tailed larva complete the development in 8
females. days and the lifecycle is completed in 17 days at
162 A.N. Shylesha and M. Mani

26 C. Mealybugs are killed by the larva of the is a tiny small wasp with yellowish body, trans-
parasitic wasp, growing inside the mealybug. parent wings and grey/bluish eyes with three
Leptomastidea can survive temperatures up to black triangular spots in the forehead. The male
40 C. parasitoid is much smaller than the female para-
sitoid. This parasitoid affects mainly the second
Acerophagus papayae stage after hatching from the egg. Each female is
It is a solitary endoparasitoid of papaya mealy- capable of laying 50 eggs in its lifetime of 35
bug Paracoccus marginatus A. It parasitizes the days. Normally, single egg is laid inside a mealy-
early-stage (II instar) nymphs of the mealybug. It bug; occasionally more than one egg is also laid.

Acerophagus papayae Leptomastidea abnormis

Anagyrus dactylopii Anagyrus indicus

It is the principal parasitoid of Nipaecoccus viri- The gregarious encyrtid parasitoid, Anagyrus
dis and Maconellicoccus hirsutus. It parasitizes indicus, oviposits in all three nymphal stages
all the nymphal instars but prefers third-instar and in the adult female stage of the spherical
nymph and adult female. They are sexually mealybug, Nipaecoccus viridis. But it prefers
dimorphic. Males are small, black with branched to the third nymphal and the adult female
antennae. Females are larger and brown in colour; mealybugs. The parasitoid development was
complete their life cycle in 15 days. the fastest, the number of parasitoids emerging
was the greatest and the ratio of female to male
Anagyrus aegyptiacus parasitoids was the highest following oviposi-
It is a solitary parasitoid of N. viridis. Females tion in the third nymphal and the adult female
deposit eggs in all the three nymphal instars and hosts.
hatch them in 4 days. There are six larval instars.
The complete life cycle covers 16 days. Anagyrus ananatis
The encyrtid A. ananatis (Subba Rao) prefers to
Anagyrus kamali parasitize adult females of Dysmicoccus brevi-
It is a solitary internal parasite of Maconellicoccus pes. It is capable of parasitizing up to 27 mealy-
hirsutus. The female deposits stalked eggs; the bugs. It can be found attacking the mealybugs in
attachment to the host derm is visible as an exter- the presence of ants, although its impact on
nal protrusion. The eggs hatch in 4 days. There mealybug mortality is low. When ants are
are six larval instars. The combined prepupal and absent, the parasitoid is highly effective in low-
pupal stages cover only 3 days. The life cycle is ering the mealybug populations in pineapple
completed in 18 days at 25 C. plantings.
13 Natural Enemies of Mealybugs 163

Anagyrus indicus Gyranusoidea tebygi

Gyranusoidea tebygi periods recorded were 18, 17, 16 and 14 days for
It is a native parasitoid of Rastrococcus invadens the rst, second, third and fourth nymphal instars,
Williams in India. The introduction of respectively. Oviposition commenced within
Gyranusoidea tebygi Noyes into Togo and Benin 24 h of emergence and lasted effectively for 6
was capable of eliminating R. invadens. It repro- days, during which 95 % of its eggs were laid and
duced on rst, second and third instars and it 1012 large hosts were killed through host feed-
avoided hosts that were already parasitized. Host ing. Sex ratio is 1:3.
feeding was occasionally observed. Sex ratios of
the offspring were male biased in smaller hosts, Aenasius bambawalei
as opposed to being female biased in larger hosts. It is a solitary endoparasitoid of Phenacoccus
Females had longer developmental times than solenopsis Tinsley in India and Pakistan. Egg and
males, developed faster in larger mealybugs than larval stages of the parasitoid are not visible
in smaller ones and were always larger than the being an internal feeder, but swelling and poor
males emerging from the same host instar. Their movement of the parasitized mealybugs were
size increased with the instar of the host at ovipo- observed after 23 days of parasitization. The
sition. About 90 % of all ovipositions in second- parasitized mealybugs transformed into dark-
and third-instar nymphs resulted from an attack brown mummies within 47 days. The pupae of
with multiple stings, starting with a sting in the A. bambawalei Hayat were barrel shaped with
head of the host for the most part. dark-brown colour. Duration of the pupal period
ranged from 5 to 8 days. Adults emerged by cut-
Apoanagyrus lopezii ting a circular small hole on the mummies after
Apoanagyrus (Epidinocarsis) lopezi (De Santis) completion of the pupal period. The adults of
is a species of the parasitic wasp native to Central both the sexes are shiny black in colour. Males
America. It is used as a biological control agent were smaller than females. The maximum devel-
against the cassava mealybug Phenacoccus mani- opmental time was recorded for the second-instar
hoti Matile-Ferrero in Africa. The parasitoid is host nymph as compared to the third instar. The
found to parasitize and complete development in males developed faster than the females in all
all developmental instars of Ph. manihoti. host stages. The overall sex ratio was 1:2. The
However, the parasitoid mortality was high maximum number of female wasps developed at
(15 %) when the development took place in the third-instar nymph (59.6 %), and it was con-
rst nymphal instar of the host. Complete devel- cluded that the third-instar host nymph appeared
opment from egg to adult emergence was pro- to be the most suitable host stage for mass
longed in smaller hosts, and the developmental rearing.
164 A.N. Shylesha and M. Mani

Clausenia purpurea Ishii supplementary role in suppressing the

It is a known parasitoid of Ps. citriculus and Ps. mealybugs.
comstocki. It attacks the rst and second mealy-
bug instars. Males are rare. Each female deposits Allotropa burrelli
about 200 eggs in 1520 days. Life cycle is com- Allotropa burrelli Mues. is a gregarious parasit-
pleted in 2530 days. oid of Pseudococcus comstocki (Kuw.), with
incubation stage averaging 9.5 days and larval
Hungariella spp. stage averaging 6.5 days. There is a single larval
H. pretiosa (Timverlake) is known to attack Ps. instar; prepupa averaging 2.0 days; pupa averag-
fraglis. It is a solitary internal parasitoid of the ing 13.0 days. The sex ratio has ranged from 2:1
second-instar mealybug nymphs. Most of 100 to 3:1, with females predominating. The adults
200 eggs per female are laid during the rst day are small and short lived, and oviposit at random
of its life. The egg enlarges eightfold before in the host body cavity. There is no preoviposi-
hatching. Incubation and larval period are 6 and tion period. All nymphal stages of the mealybugs
17 days, respectively. The life cycle is completed are attacked, but a preference is shown for those
in 23 days. Sex ratio is 1:1. H. peregrina at least half grown. The life cycle ranges from 26
(Compere) is attacking Ps. longispinus. to 38 days, with an average of 31 days.

Anarhopus sydneyensis Timberlake Allotropa citri

It is native of Australia known to parasitize Ps. It can parasitize all stages of Pseudococcus cryp-
longispinus. It is a solitary parasitoid preferring tus. It prefers the rst- and the second-instar
to attack the third-instar nymphs and the life nymphs. The lower developmental threshold
cycle covers 1 month. temperature and thermal constant of A. citri for
the rst- and second-instar nymphs of P. cryptus
Tetracnemoidea inica (Ayyar) were 10.1 C and 518.1 degree-days (DD),
It is a solitary parasitoid of Planococcus lilaci- respectively.
nus. It attacks all the nymphal instars but prefers
5-day-old nymphs, which yielded higher number Allotropa suasaardi
of parasitoids and also female progenies. It takes Allotropa suasaardi Sarkar and Polaszek is a par-
2633 days to complete the life cycle (Mani and asitoid of Phenacoccus manihoti Matile-Ferrero
Krishnamoorthy 1995). on cassava in Thailand. The mean developmental
time was shorter and a higher number of progeny Platygastridae were produced in Dysmicoccus neobrevipes fol-
Parasitoid wasps, belonging to the hymenopteran lowed by Ph. manihoti.
family Platygastridae (sometimes incorrectly
spelled Platygasteridae), are mostly very small Allotropa japonica
(12 mm), black and shining, with elbowed Allotropa japonica is a platygastrid parasitoid of
antennae that have an eight-segmented agellum. Maconellicoccus hirsutus (Green). It oviposits on
The wings most often lack venation, though they all the three nymphal stages and the adult female
may have slight fringes of setae. Several species mealybugs. Freshly laid eggs of A. japonica are
of the genus Allotropa are known to attack very small, elongated, whitish and transparent.
mealybugs. They complete the life cycle in 25 They become more or less spherical after 24 h.
days at 25 C. It oviposits on all the three nymphal Incubation period ranges from 4 to 6 days, the
stages and on the adult female mealybugs. It pre- average being 5.5 days. Usually one to three eggs
fers 1015-day-old mealybugs (second and early are found in a parasitized mealybug. The larval
third instar nymphs) for parasitization. Adults are development is completed in 46 days, there is
small and short lived (Mani and Krishnamoorthy but one larval instar with ten body segments.
1989; Clancy 1944; Gilliat 1939). They play a Prepupal and pupal periods last for 23 days and
13 Natural Enemies of Mealybugs 165

1290 days, respectively. The total life cycle of Adult aphelinids may feed on honeydew
A. japonica sp. n. is completed in 25.5 days. exuded by their hosts or on secretions issuing
Adults are small and short-lived. Longevity of from the wound caused during oviposition. The
the adults ranges from 7 to 11 days. The males eggs of aphelinids are often stalked. A number of
have long, hirsute, moniliform antennae, while endoparasitic species have an apneustic caudate
the females have shorter and distinctly clavate primary larva. Those that are endoparasitoids
antennae. Mating and oviposition takes place (e.g. Coccophagus) have larvae with neither spir-
readily. The adults exhibit a very good searching acles nor a functioning tracheal system. Some
capacity. A maximum of 238.16 parasitoids was species pupate inside the living host within a
obtained when the third-instar nymphs of 15 days pupation chamber, which becomes lled with air.
old were offered to A. japonica sp. n. for parasit- There is some evidence that the air inside this
ization (Mani and Krishnamoorthy 1989) chamber is derived from the hosts tracheal sys-
tem as in the Encyrtidae. Parasitoids emerge by
Allotropa utilis Muesbeck cutting a hole through the integument of the host
It is an internal, solitary parasitoid of nymphs of mummy; but if the mealybug has a delicate cov-
Phenacoccus aceris (Signoret) and Ph. pergandi ering, they push their way out from beneath it.
Ckll, native of Nova Scotia. It is reported to have The adults of some such species lack functional
a single generation. It attacks the smaller nymphs mandibles. Overwintering is normally as a
from July to October. Eggs laid in the body uid mature larva or pupa. The Aphelinidae are very
of the mealybugs increase sixfold during incuba- unusual in that the males and females may have
tion. Overwintering is by immature larvae in the different ontogenies. The females of such species
parasitized mealybugs. Pupation occurs in the always develop as primary endoparasitoids of
spring. The adult emergence takes place in May mealybugs.
from the overwintering host nymphs.
Coccophagus gurneyi Aphelinidae It is quite polyphagous and is native of Australia.
Along with Encyrtidae, this family provides It is a solitary internal parasitoid of all the
most of the biocontrol agents. Aphelinids are nymphal instars of Ps. fragilis, Ps. comstocki and
small, soft-bodied parasitic wasps, yellow or Ps. longispinus. Coccophagus gurneyi Compere
brown in colour and do not typically exceed has a complex developmental biology. The
1.5 mm in length. The larvae of the majority are female-producing eggs are laid free in the body
the primary parasitoids on mealybugs. They are uids of the mealybug, where they hatch in about
found throughout the world in virtually all habi- 4 days at 27 C. The larva develops in 10 days
tats and are extremely important as biological followed by a 2-day prepupal stage and an 11-day
control agents. With regard to their biology, pupal stage. The total duration goes up to 44
Aphelinidae more closely resemble Encyrtidae. days. The male-producing egg of the parasitoid is
Characters uniting the family Aphelinidae are not deposited in the developing larva of the female
apomorphic; that is, they are not uniquely parasitoid. It gave a good control of Ps. fragilis in
derived. The characters of Aphelinidae are com- South Africa and Chile.
plete notaular lines of the mesoscutum; trans-
verse or broad petiole (propodeum); long Other Families
marginal; short stigma; and short or absent post- There are species belonging to the families
marginal wing veins; and third valvula distinctly Braconidae, Eucoilidae, Signiphoridae,
separated and articulated with third valvifer. Eulopidae and Pteromalidae that are known to
These character combinations might also serve to attack the mealybugs but are of minor importance
differentiate Aphelinidae from other families of (Table 13.2).
166 A.N. Shylesha and M. Mani

Table 13.2 List of some important encyrtid parasitoids of mealybugs

Parasitoid Mealybug
Hymenoptera, Encyrtidae Maconellicoccus hirsutus
Anagyrus kamali Moursi
Apoanagyrus (Epidinocarsis) lopezi (De Santis) Phenacoccus manihoti
Anagyrus ananatis Gahan Dysmicoccus brevipes
Hambletonia pseudococcina Compere D. brevipes
Anagyrus aegyptiacus Moursi Nipaecoccus viridis
Anagyrus dactylopii (Howard) M. hirsutus and N. viridis
Anagyrus pseudococci (Gir.) Planococcus citri
Anagyrus fusciventris (Girault) Pseudococcus longispinus
Anagyrus loecki Noyes and Menezes Paracoccus marginatus and Phenacoccus madeirensis
Anagyrus punctulatus Agarwal Saccharicoccus sacchari
Anagraphus sp. P. citri
Pseudectroma sp. Pseudococcus viburni
Acerophagus maculipennis (Mercet) Pseudococcus viburni
(Pseudaphycus maculipennis)
Acerophagus notativentris (Girault) Ps. longispinus
Arhopoideus peregrinus (Compere) Ps. longispinus
Anarhopus sydneyensis Timberlake Ps. longispinus
Leptomastidea abnormis (Girault) Pl. citri
Leptomastix dactylopii Howard Pl. citri
Leptomastix epona (Walker) Pseudococcus afnis and Spilococcus cactearum
Pseudleptomastrix mexicana Noyes and Schauff Pa. marginatus
Praleurocerus viridis (Agarwal) Rastrococcus iceryoides
Pseudaphycus phenacocci Yasnosh Phenacoccus mespili
Pseudaphycus utilis Timberlake Nipaecoccus nipae
Pseudaphycus malinus Gah. Ps. comstocki
Pseudaphycus angelicus (Howard) Pseudococcus maritimus
Acerophagus notativentris (Girault) Pseudococcus maritimus
Apoanagyrus (Epidinocarsis) lopezii De Santis Phenacoccus manihoti
Gyranusoidea tebygi Noyes Rastrococcus invadens
Gyranusoidea indica Shafee, Alam and Agarwal M. hirsutus
Praleurocerus viridis (Agarwal) Rastrococcus icerioides
Acerophagus papayae Noyes and Schauff) Paracoccus marginatus
Aenasius bambawalei Hayat Penacoccus solenopsis
Aenasius advena Comp. F. virgata
Aenasius abengouroui (Risbec) Planococcus njalensis
Cheilonerus sp. M. hirsutus
Alamella ava (Agarwal) M. hirsutus
Tetracnemoidea indica Ayyar Planococcus lilacinus
Acroaspidia myrmicoides (Comp and Zinna) F. virgata
Blepyrus insularis (Camp.) F. virgata
Bothriocraera bicolor (Comp and Zinna) F. virgata
Chrysoplatycerus splendens How. F. virgata
Neodiscodes martini Comp. F. virgata
Neodusmetia sangwani (Subba Rao) Antonina graminis
13 Natural Enemies of Mealybugs 167

Table 13.2 (continued)

Parasitoid Mealybug
Tananomastix abnormis Gir. F. virgata
Zarhopalus inquisitor How. F. virgata
Neodusmetia sangwani (Subba Ra) Antonina graminis
Rhopus nigroclavatus (Ashmead) Brevennia rehi
Leptomastix nigrocincta Risbec Coccidohystrix insoilta
Leptomastix nigrocoxalis Compere Coccidohystrix insoilta
Leptomastix epona (Walker). Spilococcus cactearum
Leptomastidea abnormis (Girault) Pl. citri
Leptomastix dactylopii How Pl. citri
Pseudleptomastrix mexicana Noyes and Schauff Pa. marginatus
Alamella ava Agarwal Pl. citri
Coccidoxenoides perminutus (Timberlake) Pl. citri
Platygasteridae Pl. citri
Allotropa citri Mues.
Alltropa japonica sp. nr M. hirsutus
Allotropa burrelli Mues. Pseudococcus comstocki
Allotropa utilis Mues. Phenacoccus aceris
Allotropa convexifrons Mues. Pseudococcus comstocki
Allotropa mecrida (Walker) M. hirsutus, P. citri
Leptacis sp. Pseudococcus sp.
Phanerotoma dentata (Panzer) M. hirsutus
Trioxys angelica Hal F. virgata
Eucoilidae M. hirsutus
Leptopilina sp.
Signiphoridae M. hirsutus
Chartocerus walkeri sp. nr.
Chartocerus spp. C. insolita
Aphelinidae M. hirsutus
Aphelinus sp.
Erioporus aphelinoides (Comp.) M. hirsutus
Coccophagus caridei (Brethes) Planococcus citri
Coccophagus sexvittatus Hayat Rastrococcus invadens
Coccophagus sexvittatus Hayat Rastrococcus iceryoides
Coccophagus gurneyi Comp. Ps. calceolariae
Coccophagus pseudococci Compere C. insolita
Eulopidae F. virgata
Syntomosphyrum zygaenarum Ferriere
Aprostocetus ajmerensis (Khan and Shafee) C. insolita
Pteromalidae F. virgata
Anysis alcocki Ashm.
Catolaccus crassiceps (Masi) C. insolita
168 A.N. Shylesha and M. Mani

13.3 Entomopathogens the mealybugs. Pathogenicity of many of the

pathogens have not been seen on mealybugs.
The wax cover and the secretion process are Some of the records might have resulted from
involved in mealybug defence against natural saprophytic growth on the dead mealybugs. A
enemies particularly the pathogens. Among the total of 13 pathogens were reported in different
microbes, only the entomopathogenic fungi are countries (Moore 1988).
recorded as causing natural infection against the Neozygites fumosa Speare was found to be a
mealybugs and these records are sparse and con- very important natural agent in regulating the
fused. The pathogens of the mealybugs appear to mealybug Phenacoccus manihoti Matile-Ferrer
be restricted as yet to the Zygomycotina and in Congo (Le Ru 1986). Development of epizoot-
Deutromycotina and the former to the class ics appeared to be inuenced by a relative humid-
Zygomycetes. The class contains two orders, ity of 90 % or more, minimum daily temperatures
namely Mucorales and Entomophthorales. greater than 20 C and the mealybug density.
Table 13.3 records a number of pathogens from Adult mealybugs are more susceptible than the

Table 13.3 List of entomopathogens and entomopathogenic nematodes recorded on mealybugs

Pathogens/nematodes Mealybugs
Fusarium pallidoroseum (Cooke) Sacc Phenacoccus solenopsis
Fusarium equiseti (Corda) Sacc Coccidohystrix insolita
Verticillium lecanii (Zimm.) Paracoccus marginatus
Lecanicillium (Verticillium) lecanii (Zimm.) Phenacoccus solenopsis, M. hirsutus
Metarhizium anisopliae (Metsch.) Sorokin Root mealybugs (Planococcus sp., Planococcus
citri, P. lilacinus, Dysmicoccus brevipes and
Ferrisia virgata
Metarhizium anisopliae Maconellicoccus hirsutus
Metarhizium sp. Dysmicoccus boninsis
Pseudomonas uorescens Migula Paracoccus marginatus
Beaveria bassiana (Bais-Criv) Vuill Paracoccus marginatus
Neozygites fumosa (Speare) P. citri, Phenacoccus sp., Phenacoccus manihoti
Cladosporium sp. Phenacoccus herreni Cox and William
Entomophthora fumosa Speare Planococcus citri
Entomophthora fresenii (Nowak.) P. citri, F. virgata, Nipaecoccus nipae
Aspergillus parasiticus Speare Saccharicoccus sacchari, Dysmicoccus boninsis,
Planococcoides njalensis (Laing)
Aspergillus fIavus Link Pseudococcus calceolariae (Maskell)
Dysmicoccus boninsis (Kuwana) Saccharicoccus
sacchari (Cockerell)
Cephalosporium sp. Planococcoides njalensis (Laing)
Cladosporium oxysporum Berk and M.A. Curtis Planococcus citri (Risso)
Conidiobolus pseudococci (Speare) Pseudococcus calceolariae
Hirsutella sphaerospora H.C. Evans and Samson Rastrococcus invadens
Entomopathogenic nematodes
Steinernema thermophilum Ganguly and Singh Phenacoccus solenopsis
Steinernema meghalayensis sp. n. Phenacoccus solenopsis
Steinernema riobrave Cabanillas, Poinar and Raulston Phenacoccus solenopsis
Steinernema harryi. sp. n. Phenacoccus solenopsis
Heterorhabditis zealandica Poinar Pseudococcus viburni
13 Natural Enemies of Mealybugs 169

immature mealybugs. Besides Neozygites cause 72 % reduction in the mealybug population

fumosa, the fungi that have been conrmed as (Pa. marginatus).
pathogenic to mealybugs are Hirsutella sphaero- Root mealybugs: Drenching of 3 % Neem
spora, Verticillium lecanii, Aspergillus parasiti- seed kernel extract (NSKE) and Verticillium leca-
cus and possibly Cladosporium oxysporum. nii Econil 7 g/L) was effective against the root
Entomophthora fumosa caused up to 58.1 % mealybugs (Smitha and Mathew 2010).
mortality of the third-instar nymphs and adult
Planococcus citri (Risso) in a period of high rain-
fall and humidity in the wet season in January 13.4 Entomopathogenic
(Murray 1978). The fungal pathogen Metarhizium Nematodes
anisopliae (Metsch.) Sorokin was found to cause
79.6 % reduction in the mealybug population, 30 Entomopathogenic nematodes (EPNs) have
days after the treatment under laboratory condi- potential for biological pest control and have
tions (Devasahayam and Koya 2000). Beauveria been successfully used in several countries in soil
bassiana (Bals.) Vuill and Metarhizium aniso- and cryptic pest control. It is hypothesized that
pliae (Metschn.) Sorokn, Lecanicillium lecanii the rarity of infestation by nematodes is related to
(Zimm.) Zare and W. Gams and Isaria fumosoro- the wax shield. Stuart et al. (1997) found a varied
seus (Wize) were found pathogenic to susceptibility of Dysmicoccus vaccinii Miller and
Maconellicoccus hirsutus Green at 15 and Polavarapu to several nematode species; they
20 C. The fungus Beauveria bassiana (Bals.- showed that the removal of the waxy coating
Criv.) Vuill. was found to cause high mortality in from the mealybug did not inuence their suscep-
short time periods in adult females of the mealy- tibility to Heterorhabditis bacteriophora Poinar.
bug Dysmicoccus texensis (Tinsley) (Andalo Heterorhabditis bacteriophora has been success-
et al. 2004). Fusarium pallidoroseum caused fully shown to kill mealybugs. Planococcus citri
8095 % mortality of Ph. solenopsis (Monga was found to be the most susceptible to
et al. 2010). The fungal pathogen Lecanicillium Steinernema yirgalemense and Heterorhabditis
(Verticillium) lecanii was found to be pathogenic zealandica, causing 97 % and 91 % mortality,
to Ph. solenopsis in Tamil Nadu (Banu et al. respectively.
2010). Cadavers of Ph. solenopsis infected with In Western Cape Province, South Africa, an
Fusarium pallidoroseum (Cooke) Sacc were col- isolate of Heterorhabditis zealandica, has
lected from Haryana and Punjab during 2007 resulted in mortality of Pseudococcus viburni
2010. In the laboratory, F. pallidoroseum caused (Signoret) up to 80 % after 48 h. All stages of P.
8095 % mortality of P. solenopsis (Monga et al. viburni beyond crawlers appeared to be suscepti-
2010). The fungal pathogen Lecanicillium ble to the nematode infection. Hence, the control
(Verticillium) lecanii was found to be pathogenic in the eld should take place when the intermedi-
to Ph. solenopsis in Tamil Nadu (Banu et al. ates and adults are most abundant (Stokwe and
2010). Malan 2010). In India, Steinernema thermophi-
In vitro application of Verticillium lecanii, lum caused 83 % mortality of the mealybug (Ph.
Beauveria bassiana, B. brongniartii and Solenopsis) within 72 h after inoculation at 50 IJ/
Metarhizium anisopliae at single dose (1 107 mL and 100 % within 48 h at 500 IJs/mL.
conidiospores/mL) against P. citri inicted a Steinernema riobrave and S. harryi n. sp. pro-
mortality of 91.1, 75.5, 66.6 and 45.3 %, respec- duced intermediate mortality of about 66 %
tively. Verticillium lecanii at ve doses (ranging within 60 h at 500 IJs/mL. Emergence was
from 1 105 to 1 109 conidiospores/mL) caused observed only in 16.6 % of the mealybug cadav-
a mortality of 45, 65, 80, 90 and 95 %, respec- ers infected with S. thermophilum and S. harryi
tively (Saranya 2008). Pseudomonas uorescens sp. nr. Entomopathogenic nematode Steinernema
Migula, a common Gram-negative, rod-shaped glaseri was also known to cause mealybug mor-
bacterium, as foliar application, was found to tality under laboratory conditions.
170 A.N. Shylesha and M. Mani

The nematode Steinernema carpocapsae Chong JH, Oetting RD (2007) Specicity of Anagyrus sp
nov nr. sinope and Leptomastix dactylopii for six
(Weiser) was found to cause high mortality in
mealybug species. Biocontrol 52:289308
short time periods in adult females of the mealy- Clancy DW (1944) Biology of Allotropa burrelli, a gre-
bug Dysmicoccus texensis (Tinsley) (Andalo garious parasite of Pseudococcus comctocki. J Agric
et al. 2004). The aqueous suspension of EPN Res 69:159167
Devasahayam S, Koya KMA (2000) Evaluation of ento-
(JPM3) was more efcient with 70 % control
mopathogenic fungi against root mealybug infesting
efciency on the root mealybug Dy. texensis black pepper. In: Abstracts, Entomocongress 2000,
(Alves et al. 2009). Heterorhabditis bacteriophora Association for Advancement of Entomology,
Poinar strain HC1 was known to cause 100 % Trivandrum, 58 Nov 2000, pp 3334
Devasahayam S, Koya KMA, Anandaraj M, Thomas T,
mortality in the inoculated coffee mealybug com-
Preethi N (2009) Distribution and bio-ecology of root
plex (Rodriguez et al. 1998). Dysmicoccus texen- mealybugs associated with black pepper (Piper
sis is an example for the coffee root mealybug. nigrum Linnaeus) in Karnataka and Kerala, India.
Greenhouse results demonstrate that the aqueous Entomon 34:147154
Dinesh AS, Venkatesha MV, Ramakrishna S (2010)
suspension (JPM3) was more efcient with 70 %
Development, life history characteristic and behaviour
control efciency. of mealybug predator Spalgis epeus (Westwood)
(Lepidoptra: Lycaenidae) on Planococcus citri (Risso)
(Homoptera: Pseudococcidae). J Pest Sci 83:339345
Gillani WA, Copland M, Raja S (2009) Studies on the
References feeding preference of brown lacewing (Sympherobius
fallax Navas) larvae for different stages of long-tailed
Alves VS, Moino Junior A, Santa-Cecilia LVC, Rohde C, mealy bug (Pseudococcus longispinus) (Targioni and
da Silva MAT (2009) Tests for the control of coffee Tozzetti). Pak Entomol 31(1):14
root mealybug Dysmicoccus texensis (Tinsley) Gilliat RC (1939) The life history of Allotropa utilis
(Hemiptera, Pseudococcidae) with Heterorhabditis Mues., a hymenopterous parasite of the orchard
(Rhabditida, Heterorhabditidae) [Portuguese]. Rev mealybug Nova Scotia. Can Entomol 1:160163
Bras Entomol 53(1):139143 Giordanengo P, Nenon JP (1990) Melanization and encap-
Andalo V, Moino Junior A, Santa-Cecilia LVC, Souza GC sulation of eggs and larvae of Epidinocarsis lopezi by
(2004) Compatibility of Beauveria bassiana with its host Phenacoccus manihoti effects of superpara-
chemical pesticides for the control of the coffee root sitism and egglaying patterns. Entomol Exp Appl
mealybug Dysmicoccus texensis Tinsley (Hemiptera: 56:155163
Pseudococcidae) [Portuguese]. Neotrop Entomol Herren HR, Neuenschwander P (1991) Biological control
33(4):463467 of cassava pests in Africa. Ann Rev Entomol
Banu JG, Suruliveru T, Amutha M, Gapalakrishnan N 36:257283
(2010) Susceptibility of cotton mealybug, Paracoccus Le Ru B (1986) Epizootiology of the entomophthoraceous
marginatus to entomopathogenic fungi. Ann Plant fungus Neozygites fumosa in a population of the cas-
Prot Sci 18(1):247248 sava mealybug, Phenacoccus manihoti (Hom,
Blumberg D (1997) Parasitoid encapsulation as a defense Pseudococcidae). Entomophaga 31:7989
mechanism in the Coccoidea (Homoptera) and its Mani M, Krishnamoorthy A (1989) Life cycle, host stage
importance in biological control. Biol Cont suitability and pesticide susceptibility of the grape
8:225236 mealybug parasitoid, Allotropa japonica sp n. J Biol
Blumberg D, Franco JC, Suma P, Russo A (2001) Control 3:79
Parasitoid encapsulation in mealybugs (Hemiptera: Mani M, Krishnamoorthy A (1990) Predation of Mallada
Pseudococcidae) as affected by the host-parasitoid boninensis on Ferrisia virgata, Planococcus citri and
association and superparasitism. Boll Zool Agr Bachic P lilacinus. J Biol Control 4:122123
SerII 33(3):385395 Mani M, Krishnamoorthy A (1991) Breeding of Blepyrus
Blumberg D, van Driesche RG (2001) Encapsulation rates insularis (Hym., Encyrtidae) on Ferrisia virgata
of three encyrtid parasitoids by three mealybug spe- (Hemip., Pseudococcidae). Entomon 16:275277
cies (Homoptera: Pseudococcidae) found commonly Mani M, Krishnamoorthy A (1995) Inuence of different
as pests in commercial greenhouses. Biol Cont stages of oriental mealybug, Planococcus lilacinus
22:191199 (Ckll.) on the development, progeny production and
Calatayud PA, Polania MA, Seligmann CD, Bellotti AC sex ratio of the parasitoid, Tetracnemoidea indica
(2002) Inuence of water-stressed cassava on Ayyar. J Insect Sci 8(2):192193
Phenacoccus herreni and three associated parasitoids. Mani M, Thontadaraya TS (1987) Biological studies on
Entomol Exp Appl 102:163175 the grape mealybug predator Scymnus coccivora
(Ayyar). J Biol Control 1:8992
13 Natural Enemies of Mealybugs 171

Mani M, Krishnamoorthy A, Sivaraju C (1991) A wonder- Sagarra LA, Peterkin DD, Vincent C, Stewart RK (2000)
ful predator. Lambert Academic Publishing, Immune response of the hibiscus mealybug,
Deutschland, 310 p Maconellicoccus hirsutus Green (Homoptera:
Monga D, Kumhar KC, Kumar R (2010) Record of Pseudococcidae), to oviposition of the parasitoid
Fusarium pallidoroseum (Cooke) Sacc. on cotton Anagyrus kamali Moursi (Hymenoptera: Encyrtidae).
mealybug, Phenacoccus solenopsis Tinsley. J Biol J Ins Physiol 46:647653
Control 24(4):366368 Saranya C (2008) Evaluation of biocontrol agents against
Moore D (1988) Agents used for biological control of Citrus mealybug Plannococcus citri. M.Sc thesis sub-
mealybugs (Pseudococcidae). Biocontrol News Inf mitted to Bharathidasn University, Tiruchirapalli
9:209225 Smitha MS, Mathew MP (2010) Management of root
Murray DAH (1978) Population studies of the citrus mealybugs, Geococcus spp. In banana cv Nendran.
mealybug, Planococcus citri (Risso), and its natural Pest Manag Hortic Ecosyst 16(2):108119
enemies on passion-fruit in south-eastern Queensland. Stokwe NF, Malan AP (2010) Potential use of entomo-
Qld J Agric Anim Sci 35(2):139142 pathogenic nematodes for biological control of
Noyes JS, Hayat M (1994) Oriental mealybug parasitoids mealybugs on apples and pears. SA Fruit J 9(3):38
of the Anagyrini (Hymenoptera: Encyrtidae). CAB 39, 42
International, Oxon, 554 p Stuart RJ, Polavarapu S, Lewis EE, Gaugler R (1997)
Rodriguez I, de Martinez de los M, Sanchez L, Rodriguez Differential susceptibility of Dysmicoccus vaccinii
MG (1998) Field comparison of the effectiveness of (Homoptera: Pseudococcidae) to entomopathogenic
Heterorhabditis bacteriophora strain HC1 for the con- nematodes (Rhabditida: Heterorhabditidae and
trol of mealybugs (Homoptera: Pseudococcidae) on Steinernematidae). J Econ Entomol 90:925932
coffee [Spanish]. Rev Prot Veg 13(3):195198
Semiochemicals in Mealybugs
N. Bakthavatsalam

A semiochemical (from Greek semeon meaning 1978). In Italy, the sex pheromone released by
signal) is a generic term used for a chemical females of Planococcus citri (Risso) was
substance or mixture that carries a message for extracted from unmated females (Rotundo and
purpose of communication. Semiochemical com- Tremblay 1976). The identication of sex phero-
munication can be divided into two broad classes: mones of several mealybug species has facilitated
communication between individuals of the same the development of monitoring techniques and
species (intraspecic) or communication between management tactics based on these compounds.
different species (interspecic). It is usually used However, experience shows that the efciency of
in the eld of chemical ecology to encompass tactics such as mass trapping, mating disruption,
pheromones, allomones, kairomones, attractants, and lure and kill may be constrained by a lack of
and repellents. Many insects, including parasitic knowledge of basic features of the life history
insects, use semiochemicals, which are natural and mating behavior of male insects and the
chemicals released by an organism that affect the mechanisms involved in their interactions with
behaviors of other individuals. Pheromones are pheromone sources. A comprehensive account of
intraspecic signals that aid in nding mates, pheromones of coccoids was provided by
food and habitat resources, warning of enemies, Dunkelblum (1999) in the book Pheromones of
and avoiding competition. Interspecic signals Non-lepidoteran Insects.
known as allomones and kairomones have similar
The existence of female sex pheromone in a 14.1 Mealybug Pheromone
coccid, Matsucoccus resinosae Bean and Characteristics
Godwin, was rst demonstrated by Doane (1966),
followed by other coccid Aonidiella aurantii These pheromones all share a number of desir-
(Makell) (Tashiro and Chambers 1967). able characteristics and also some undesirable
Identication and synthesis of sex pheromone characteristics for use in pheromone trapping.
in A. aurantii became a turning point in the pher-
omone research for the coccoids (Roelofs et al. Sex pheromones are very powerful attractants
for male mealybugs. The males hide and live
in protected areas and are not harmed by the
N. Bakthavatsalam (*) insecticides. Using pheromones even small
National Bureau of Agriculturally Important Insects, populations can be detected at earlier stages of
Bangalore 560024, India occurrence.

Springer India 2016 173

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_14
174 N. Bakthavatsalam

The standard rubber septum-type pheromone pressure is high. When used in management
lures remain attractive for 23 months under systems, they are often combined with neonic-
eld conditions, minimizing the number of otinoids, insect growth regulators, or other
lure changes required throughout one season. biopesticides.
The lures require only a tiny dose of phero- Pheromone traps were used to determine, for
mone (0.025 mg or less), which will help to example, mealybug species composition,
keep lure manufacturing costs down. relative seasonal abundance, and density. In
The chemical structure of each pheromone is the vineyards infested with mixed mealybugs,
different; therefore, each pheromone speci- using traps activated with pheromones, it was
cally attracts only its own species. Sometimes found that Planococcus cus was more
in the orchards with more than one mealybug abundant than Planococcus citri in Italy (Ortu
species, pheromones could be combined to et al. 2006).
lure or to attract several species simultane- The ability of the pheromone control pro-
ously (Waterworth et al. 2011). grams to target a specic pest and not harm
Multi-season plastic Delta traps are sugested pollinator bees and benecial insects pays big
for monitoring and mass trapping most inva- dividends.
sive insect pests. This can also be an advantage and a disadvan-
Most pesticides require direct contact with the tage that mealybugs have been caught in traps
mealybug; hence, it will not be effective located over one quarter mile from the nearest
against those under the bark. Many of the known infestation.
softer insecticides are not able to penetrate The sensitivity of the multiplex polymerase
the waxy exterior; however, pheromones are chain reaction (PCR) to identify adult males
volatile molecules dispersed through the air collected in pheromone traps was shown, with
and sensed by the insect without requiring reliable identication of Pl. cus aged for 6
penetration-reach target spot. days in pheromone traps (Daane et al. 2011)
A possible alternative to visual sampling, which
may both decrease monitoring time and increase
the sensitivity of mealybug detection meth- 14.2 Techniques for Isolation
ods, is the use of pheromone-baited traps. of Pheromones
Specically, pheromone traps were more sensi-
tive than visual methods for detecting mealybug The pheromones of moths, due to their larger
infestations. The number of insects caught on size, were easily identied using the electrophys-
traps was correlated with mealybug abundance iological and analytical techniques; however, it is
in the eld indicating that pheromone traps difcult to identify the pheromones from mealy-
can be used in place of laborious, and annual bugs mainly due to their smaller size and avail-
sampling to monitor the mealybug populations. ability in lesser quantity of pheromones. Large
A second benet of the pheromone use over numbers of virgin females of mealybugs were
conventional broad-spectrum pesticides was required for the extraction of the female sex
that the ecological balance and natural preda- pheromone (Rotundo and Tremblay 1976). The
tor populations were preserved. Secondary large-scale production of mealybugs is done on
pest populations often surge later in the season potato sprouts or ripe pumpkins in several coun-
when broad-spectrum pesticides are used tries (Smith and Armitage 1920; Joshi et al. 2010;
because the pesticides kill natural predators Ahmad and Ghani 1970; Chacko et al. 1978).
of the primary pest, but with the use of phero- Behavioral attributes such as age of the calling
mones pest resurgence was contained. females and inuence of photo/scoto phases and
Vine mealybug pheromones are often inte- host plants complicate the process of pheromone
grated into pest management systems, particu- identication in mealybugs. For the isolation
larly for the rst several years when pest and identication of coccoid sex pheromones,
14 Semiochemicals in Mealybugs 175

continuous mass rearing of virgin females is might be the translucent pores on the hind legs
required, along with the sufcient numbers of coxae (metathoracic legs) (Gullan and Kosztarab
males for bioassays. Sexual separation of males 1997). The source of pheromone gland was sus-
was done either through the mechanical separa- pected to be the abdominal glands for several
tion using a water spray/brush or through the species of mealybugs. The pygidial glands were
application of juvenoids, which selectively pre- identied as the pheromone-producing glands,
vent male maturation. Pheromone production in the secretions of which are released through the
virgin females of Pseudococcus calceolariae was anus via a fragile duct. The production of phero-
not appreciably affected by the juvenile hormone mone and the response of the males to the phero-
treatment (Rotundo 1978). Compounds such as monal glands vary with the rearing conditions.
dichlorvos, triprene, RO 103108, etc. have been Feral mealybugs produce and respond to com-
used for the collection of females. pound 1, whereas lab-reared adults reared on
As a rst stage in research on the nature of potato sprouts produce and respond to both the
the female sex pheromone of the citrus pest compounds (Zada et al. 2003). For the collection
Pseudococcus calceolariae, a method was of pheromone, entrapment method using adsor-
described for collecting and extracting the phero- bent compounds such as tenax, Porapak Q or
mone from the air above virgin females reared on cold trapping was followed. The pheromone
potato sprouts in the laboratory; virgin females gland extracted with glacial acetic acid or abso-
sexed by insect growth regulators (which pre- lute ethanol was the most attractive pheromone
vented the development of males) and main- formulation for Planococcus citri (Hwang and
tained with or without food produced pheromones Chu 1987b). The plants that release volatiles
for about 16 days. Out of three absorbent materi- (such as lemon) need to be avoided as laboratory
als tested, Poropak Q proved to be the most effec- host to keep away the possible interference of
tive in absorbing the pheromone, which was these plant volatiles in the pheromone collection.
eluted from it with ethyl ether and concentrated Potato tubers or potato sprouts are considered to
by distillation or evaporation of the solvent in be the best rearing media for the collection of
nitrogen and the active fraction was subjected to pheromone.
gasliquid chromatography. All pheromone sam-
ples were evaluated by bioassay on the Poropak
in an olfactometer into which males were intro- 14.4 Behavior of Male Mealybugs
duced, or on lter paper in a petri dish containing
males (Rotundo et al. 1979a, b). In the course of The male mealybugs are known to y about one-
rearing Pseudococcus comstocki (Kuw.) on ripe half mile. The adult males usually respond to the
pumpkins in a laboratory in Japan, it was found pheromone gland secretions, and this was con-
possible to separate the sexes by the simple expe- rmed through electrophysiological and behav-
dient of wrapping the pumpkins on which the ioral studies. The daily rhythms of pheromone
mealybug was being reared in a double-folded production and the responsiveness of males were
sheet of tissue paper. Only the male nymphs very important. The males of P. citri were inac-
crawled into the paper. Adult males crawled out tive in scotophase but were very active for 30 min
from the papers and began to y soon after a after the beginning of photophase. However, the
lamp was lit (Negishi et al. 1980a). activity ceased after exposure to light. Besides
the adult males, immature stages of mealybugs
also respond to the pheromones of the female.
14.3 Pheromone Glands Second-instar nymphs of mealybugs (Pl. citri,
Ps. cryptus, N. viridis, and Pl. cus) responded to
The site of production and release of sex phero- the conspecic female sex pheromone directing
mones in female mealybugs have not yet been the males themselves to a suitable pupation site
determined, although it has been suggested that it near conspecic non-sibling mature females,
176 N. Bakthavatsalam

thus preventing in breeding. Male nymphs are Males of Pl. citri, Pl. cus, and Ps. comstocki are
not attracted to heterospecic female phero- morning iers, whose ight begins just after sun-
mones; the repellency of heterospecic sex pher- rise (Moreno et al. 1972, 1984; Ortu and Delrio
omones to males directed to look for a pupation 1982; da Silva et al.2009a, b, c; Zada et al. 2008);
site to avoid close contact with heterospecic males of Maconellicoccus hirsutus and
females (Mendel et al. 2003, 2012). Pheromotypes Nipaecoccus viridis (Newstead) y mainly
were also known to occur in Planococcus cus around sunset (Francis et al. 2007); and males of
(Signoret) (Kol-Maimon et al. 2010). The males Ps. calceolariae y both in the early morning and
of Pseudococcus calceolariae on citrus were able late afternoon (Rotundo and Tremblay 1976).
to move against the wind in a zigzag progression Moreno et al. (1984) suggested that the daily
(a klinotactic response), even in the absence of cycle of Pl. citri male ight activity is determined
pheromones. In still air, they responded to the by the scotophase period and its onset in response
pheromone source (a wad of cotton wool bearing to exposure to light. In light of the ndings of
100 u l of an ether extract of females), from Moreno et al. (1984) and O. Bar-Shalom and
within a radius of about 3 cm. In the presence of Z. Mendel (unpublished data), an endogenous
wind at the optimal speed (0.5 m/s) carrying the circadian rhythm, imprinted by the photoperiod,
pheromone, they moved directly toward the pher- may also be involved. Recently, Mendel et al.
omone source, even from a distance of over 1 m (2008) and da Silva et al. (2009a, b, c) studied
(a tropotactic response) (Rotundo et al. 1980). seven mealybug species of the genera
The turntable olfactometer method appeared to Planococcus, Pseudococcus, and Nipaecoccus to
be the most efcient to study the attractiveness of estimate for how long and at which physiological
the female sex pheromone of Planococcus citri age the mealybug males are sexually active.
to adult males. Forty 618-day-old females pro- Adult males take 3040 h to achieve sexual
vided a sufcient pheromone source, and red maturity before being able to y or to mate. Most
color sticky card was the most attractive. During mature males live for 23 days, during which
the scotophase, there was little ight by males; mating opportunities may be continuously avail-
they were attracted to the pheromone with an able, but searching for a mate by ight is limited
obvious peak within 30 min after the beginning to 24 h per day. The nding that mealybug
of the photophase. Male activity ceased 2 h after males appear to y only after exposure to day-
exposure to light (Hwang and Chu 1987b). The light suggests that visual cues also may be
responses of males to the extracted fractions involved in male ight and mate location.
showed that virgin females of both species Findings of recent experiments aimed at studying
Pseudococcus calceolariae and Planococcus the effects of the color and design of sticky traps
citri had no circadian rhythm of sexual activity baited with sex pheromone on male captures sup-
but emitted the pheromone consistently and con- port this hypothesis (Franco et al. 2008a). The
tinuously throughout the day until mated lack of simple eyes in apterous males of poly-
(Rotundo and Tremblay 1980). morphic species of mealybugs, such as S. sac-
chari (A 1968), is also an indirect evidence
that vision might be involved in male mealybug
14.5 Male Flight and Mate ight and mate location. As in other neococcoid
Location families, mealybug males typically have a pair of
dorsal and ventral simple eyes plus a pair of
In light of the pattern observed among the few smaller lateral ocelli (A 1968; Gullan and
species whose sex pheromones were identied, Kosztarab 1997). There is a lack of clear knowl-
mate location by mealybug males seems to rely edge about the functional aspects of this bizarre
mainly on chemical cues, that is, adult females of visual system. Duelli (1985) suggested that the
biparental mealybug species utilize sex phero- eyes in scale insect males are positioned in a
mones to attract males (Dunkelblum 1999). horizontal ring around the head because the
14 Semiochemicals in Mealybugs 177

males body axis is maintained almost vertical bug Pseudococcus viburni (Millar et al. 2005b),
during ight. The main purpose of the eyes would grape mealybug Pseudococcus maritimus
be to monitor the presence of females in conjuc- (Ehrhorn) (Figadre et al. 2007), passionvine
tion with pheromones. mealybug Planococcus minor (Maskell) (Ho
Unlike neotenic adult females, male mealy- et al. 2007), Japanese mealybug Planococcus
bugs are active iers, do not feed, and they live kraunhiae (Kuwana) (Sugie et al. 2008), long-
only a few days. The response of males of differ- tailed mealybug Pseudococcus longispinus
ent ages to a synthetic pheromone and virgin (Millar et al. 2009), Madeira mealybug,
females was tested. In the petri dish bioassay, Phenacoccus madeirensis Green (Ho et al. 2009),
class I males (up to 10 h after eclosion) and less citrophilous mealybug Planococcus calceolariae
than 20 % of class II males (1029 h after eclo- (Maskell) (El-Sayed et al. 2010) and Dysmicoccus
sion) responded to the pheromone or virgin grassii Leonardi (de Alfonso et al. 2012).
females. On the other hand, most of class III All known mealybug pheromones are mono-
males (29 or more hours after eclosion) showed a terpenoid esters, mostly of simple acids.
clear response. After eclosion, most P. citri males However, most of them are irregular non-head-
need to complete a period of sexual maturation of to-tail monoterpenoids, with unusual connections
at least 30 h before they can respond to the sex of two isoprene units (Millar and Midland 2007).
pheromone and mate. Without mating, the maxi- The majority of naturally occurring isoprenoid
mal lifespan of males was approximately 5 days compounds that have been identied have
and 50 % of males lived only up to 4.4 days 14,head-to-tail linkages between isoprenoid
(25.0 0.5 C). Most P. citri males have less than units, whereas most irregular terpenoids with
3 days to nd a receptive female and mate with non-head-to-tail linkages have been found in
her. However, since P. citri males only y within a members of the plant family Asteraceae (Rivera
period of approximately 4 h after sunrise, the total et al. 2001). Non-head-to-tail isoprenoid com-
effective time available for mate location by ight pounds are produced in three biosynthetic reac-
is only less than 12 h (da Silva et al. 2009a, b, c). tions, that is, cyclopropanation, branching, and
cyclobutanations (Thulasiram et al. 2008). Millar
and Midland (2007) suggested that terpenoid bio-
14.6 Identication/Isolation synthetic pathways in mealybugs are distinctly
of Pheromones different from the typical terpenoid pathways
found in other organisms, representing a variety
Using sophisticated analytical and bioassay of enzymes that can catalyze cyclizations and
instruments such as gas chromatographymass rearrangements. On this basis, and considering
spectral detector (GCMS), gas chromatography that mealybug endosymbionts are believed to be
electroantennogram detector (GCEAD), vibra- important to the nitrogen and sterol requirements
tional circular dichroism (VCD) spectroscopy, of their hosts and may play a role in physiologi-
and nuclear magnetic resonance (NMR) spec- cal processes such as resistance to microbial
troscopy, the sex pheromones of some economi- pathogens or detoxication of plant secondary
cally important species of mealybugs have been compounds, we tend to speculate that these
identied and synthesized. These include the enzymes may originate, at least in part, from
Comstock mealybug Pseudococcus comstocki mealybug endosymbionts. Thus, for example, a
(Negishi et al. 1980b), citrus mealybug variety of symbionts associated with bark beetles
Planococcus citri (Bierl-Leonhardt et al. 1981), are capable of producing compounds that are
vine mealybug Planococcus cus Signoret used as pheromones. Spectroscopically, phero-
(Hinkens et al. 2001), citriculus mealybug mones have been isolated and identied from
Pseudococcus cryptus Hempel (Arai et al. 2003), several species of mealybugs. A list of phero-
pink hibiscus mealybug Maconellicoccus hirsu- mones identied for several species is given in
tus (Green) (Zhang et al. 2004), obscure mealy- Table 14.1.

Table 14.1 Pheromone compounds identied from different species of mealybugs

Sl. No. Species Chemical identied Identication reference Synthesis references
1 Crisicoccus matsumotoi 3-methyl-3-butenyl-5-methyl-hexanoate Tabata et al. (2012) Tabata et al. (2012)
2 Maconellicoccus hirsutus Trans-1R,3R-chrysanthemyl (R)-2-methyl Zhang et al. (2004) Zhang et al. (2004); Zhang and Nie (2005)
(Green) butanoate and (R) lavandulyl (R) methyl
butanoate (93:1)
(R)-2-isopropenyl-5-methyl-4-hexenyl Zhang and Nie (2005)
(S)-2-methylbutanoate [common name is
(R)-lavandulyl (S)-2-methylbutanoate] and
cyclobutyl]methyl (S)-2-methylbutanoate
[which we refer to as (R)-maconelliyl
3 Phenacoccus madeirensis Trans (1R,3R)-chrysanthemyl (R)-2-methyl- Ho et al. (2009)
Green butanoate and (R)
4 Planococcus citri (Risso) (+)-(1R)-cis-2,2,-dimethyl 3-isopropenyl Bierl-Leonhardt et al. Kukovinets et al. (2006); Zada et al. (2004); Passaro and
cyclobutane methanol acetate (1R,3R) (1981, 1982) Webster (2004); Chibiryaev et al. (1991); Odinokov et al.
3-isopropenyl-2,2-dimethyl cyclobutane (1991); Serebryakov et al. (1986); Wolk et al. (1986);
methyl acetate Odinokov et al. (1984a, b); Carlsen and Odden (1984);
Bierl-Leonhardt et al. (1981)
5 Planococcus minor E-2-isopropyl-5-methyl-2-hexadienyl acetate Ho et al. (2007) Millar (2008); Ho et al. (2007)
6 Planococcus cus S-lavandulol and (S)-(+)-lavandyl senecioate Hinkens et al. (2001); Ujita and Saeki (2008); Zada and Dunkelblum (2006);
(Signoret) Zada et al. (2001); Zada and Harel (2004); Zada et al. (2003), Millar et al.
Zada et al. (2003) (2002), Hinkens et al. (2001)
7 Pseudococcus comstocki R-3-acetoxy,2,6-dimethyl-1,5,-heptadiene Negishi et al. (1980b) McCullough et al. (1991); Baeckstroem and Li (1990);
(Kuwana) 2,6-dimethyl-1,5-heptadien-3-yl acetate Bichina et al (1982) Kang and Park (1990); Skatteboel and Stenstroem (1989);
Larcheveque and Petit (1989); Fall et al. (1986);
Baeckstrom et al. (1984); Nakagawa and Mori (1984);
Bierl-Leonhardt et al. (1982); Mori and Ueda (1981);
Uchida et al. (1981)
N. Bakthavatsalam
Sl. No. Species Chemical identied Identication reference Synthesis references

8 Pseudococcus cryptus (1R3R)-3-isopropenyl-2-2- Arai et al. (2003) Nakahata et al. (2003)

Hempel dimethmylcyclobutylmethyl-3-methyl-3-
9 Pseudococcus Chrysamthemyl 2-acetoxy-3-methylbutanoate Unelius et al. (2011); Unelius et al. (2011); El-Sayed et al. (2010)
calceolariae (Maskell) El-Sayed et al. (2010)
10 Pseudococcus maritimus (R, R)-trans-(3,4,5,5-tetramethyl cyclopent-2- Figadre et al. (2007) Figadre et al. (2007)
(Ehrhorn) en-1-yl) methyl 2-methyl propanoate
11 Pseudococcus viburni (1R,2R,3S)-(2,3,4,4-tetramethyl cyclopentyl)- Millar et al. (2005b) Hashimoto et al. (2008); Millar and Midland (2007)
(Signoret) methyl acetate
12 Pseudococcus kraunhiae 2-isopropylidene-5-methyl-4-hexen-1-yl Sugie et al. (2008)
(Kuwana) butyrate
Semiochemicals in Mealybugs

13 Pseudococcus longispinus 2-(1,5,5-trimethylcyclopent-2-en-1-yl)ethyl Millar et al. (2009) Millar et al. (2009)

(Targioni Tozzetti acetate
14 Planococcus minor 2-isopropyl-5-methyl-2,4-hexadienyl acetate Ho et al. (2007) Ho et al. (2007)
15 Dysmicoccus grassii ()-(R)-lavandulyl propionate and acetate de Alfonso et al. (2012)
180 N. Bakthavatsalam

14.6.1 Planococcus citri 14.6.3 Planococcus kraunhiae

In Italy, the sex pheromone released by females A sex pheromone component of the Japanese
of Planococcus citri was extracted from unmated mealybug, Planococcus kraunhiae was isolated
females by ethanol, diethyl ether, or petroleum and identied. A crude extract of the pheromone
ether. Extracts in ethanol, diethyl ether, or petro- obtained by airborne collection was rst fraction-
leum ether placed on lter paper or hydrophilized ated with Florisil column chromatography. The
poly(methyl methacrylate) discs elicited high active fraction was further puried by HPLC, and
attraction and pairing responses in the males an active component was isolated by preparative
(Rotundo and Tremblay 1976, 1982). P. citri GC. The purified compound was determined
pheromone is a cyclobutane compound. to be 2-isopropylidene-5-methyl-4-hexen-1-yl
butyrate by GCMS and NMR analyses showing
the attraction activity to adult males of P.
14.6.2 Pseudococcus calceolariae kraunhiae in the eld (Sugie et al. 2008).

Headspace volatiles collected from virgin

females of the citrophilous mealybug, Ps. calceo- 14.6.4 Planococcus cus
lariae, containing the main female-specic
compound is identied as [2,2-dimethyl-3-(2- The existence of pheromones was detected in the
methylprop-1-enyl)cyclopropyl]methyl 2-ace- females of mealybugs Planococcus cus
toxy-3-methylbutanoate (chrysanthemyl (Signoret) by Rotundo and Tremblay (1982). The
2-acetoxy-3-methylbutanoate). The other two sex pheromone of Planococcus cus has been
compounds are identied as [2,2-dimethyl-3-(2- identied as a single component, (S)-lavandulyl
methylprop-1-enyl)cyclopropyl]methanol (chry- senecioate (LS) 2a. Males were equally attracted
santhemol) and [2,2-dimethyl-3-(2-methylprop to either (S)-2a or racemic 2a, indicating that the
-1-enyl)cyclopropyl]methyl 2-hydroxy-3-meth- unnatural enantiomer does not inhibit male behav-
ylbutanoate (chrysanthemyl 2-hydroxy-3-methyl ioral responses. Female mealybugs also produced
butanoate). Traps baited with 100 g and 1,000 (S)-lavandulyl, but mixtures of racemic 1 with
g indicated that 100 g of chrysanthemyl 2-ace- racemic 2a were less attractive to male mealybugs
toxy-3-methylbutanoate captured 4- and 20-fold than racemic 2a alone. In eld trials, lures loaded
more males than traps baited with virgin females with 100 g doses of racemic 2a attracted males
(El-Sayed et al. 2010). The absolute congura- for at least 12 weeks (Millar et al. 2005a).
tion of the sex pheromone of Pseudococcus
calceolariae was determined to be (1R,3R)-[2,2-
dimethyl-3-(2-methylprop-1-enyl)cyclopropyl] 14.6.5 Phenacoccus madeirensis
methyl (R)-2-acetoxy-3-methylbutanoate NMR,
derivatization reactions, chiral GCMS, and com- Two compounds in Ph. madeirensis Green were
parison with synthetic chiral reference com- identied as trans-1R, 3R-chrysanthemyl (R)-2-
pounds were used to determine the absolute methyl butanoate and (R) lavandulyl (R)-methyl
conguration of this compound. Traps baited butanoate in a ratio of 3:1. The structures of two
with 1,000 g of the pheromone compound pheromones differ signicantly.
caught 367 times more males than traps baited
with virgin females. A mixture of stereoisomers
of pheromones can be used for eld trapping 14.6.6 Pseudococcus comstocki
without adverse effects on trap catches (Unelius
et al. 2011). Pseudococcus comstocki pheromone is an aliphatic
acetate. The sex pheromone produced by females
of the Ps. comstocki Kuwana, was isolated and
14 Semiochemicals in Mealybugs 181

identied as 2,6-dimethyl-3-acetoxy-1,5-hepta- Captures of male M. hirsutus showed that phero-

diene. Synthetic pheromone showed a potent mone with the naturally occurring (R)-maconelliyl
activity in laboratory bioassay and eld test (S)-2-methylbutanoate and (R)-lavandulyl (S)-2-
(Negishi et al. 1980b). methylbutanoate [R-S conguration] was most
attractive and that pheromone with the unnatural
S-S conguration was less attractive. An inhibi-
14.6.7 Pseudococcus maritimus tory effect was observed when R-R and S-R were
combined with naturally occurring R-S blend.
In Pseudococcus maritimus (Ehrhorn), an irregu- Thus, S conguration on the acid moiety elicits
lar non-head-to-tail monoterpenoid was identi- attraction, whereas the R conguration induces
ed as (R,R)-1-trans 3,4,5,5,-tetramethyl inhibition. However, the attractive activity shows
cyclopenta-2-en-1-yl) methyl-2-methyl propi- some degree of tolerance toward chirality change
onoate (Figadere et al. 2007) and Zou et al. in the alcohol portion of the pheromone molecules
(2010) observed that racemic mixture of trans- (Zhang et al. 2006).
alphanecrodyl isobutyrate is more attractive than
(RR) or (SS) enantiomers.
14.6.11 Planococcus minor

14.6.8 Pseudococcus longispinus The sex pheromone of the mealybug, Planococcus

minor, was isolated by fractionation of crude
The sex pheromone of the long-tailed mealybug pheromone extract obtained by aeration of virgin
Ps. longispinus, identied as 2-(1,5,5-trimethylc females. The pheromone was identied as the
yclopent-2-en-1-yl)ethyl acetate, represents the irregular terpenoid, 2-isopropyl-5-methyl-
rst example of a new monoterpenoid skeleton. 2,4-hexadienyl acetate, by mass spectrometry,
A [2,3]-sigmatropic rearrangement was used in a microchemical tests, and (1)H NMR spectros-
key step during construction of the sterically con- copy. The stereochemistry of the pheromone was
gested tetra alkyl cyclopentene framework assigned as (E) by comparison with synthetic
(Millar et al. 2009). standards of known geometry. The compound
was highly attractive to males in laboratory bio-
assays, whereas the (Z)-isomer appeared to
14.6.9 Crisicoccus matsumotoi antagonize attraction (Ho et al. 2007).

Most of the mealybug pheromones are carboxyl

esters of monoterpene alcohols; however, a hemi- 14.6.12 Pseudococcus viburni
terpene pheromone (3)-methyl-3-butenyl 5 meth-
ylhexanoate was identied from Crisicoccus The sex pheromone of the obscure mealybug, Ps.
matsumotoi (Siraiva) (Tabata et al. 2012). viburni, consists of (1R*,2R*,3S*)-(2,3,4,4-
tetramethylcyclopentyl)methyl acetate, the rst
example of a new monoterpenoid structural motif
14.6.10 Maconellicoccus hirsutus in which the two isoprene units forming the car-
bon skeleton are joined by 22 and 34 con-
The two chiral centers in the sex pheromone of nections rather than the usual 14 head-to-tail
pink hibiscus mealybug, Maconellicoccus hirsu- connections. This highly irregular terpenoid
tus, could elicit different male responses. The chi- structure, and the irregular terpenoid structures of
ral center in the acid moiety of the pheromone related mealybug species, suggests that these
seemed to be more critical than the alcohol portion insects may have unique terpenoid biosynthetic
of the pheromone molecule for attractiveness. pathways (Millar et al. 2005b).
182 N. Bakthavatsalam

14.6.13 Dysmicoccus grassii cated and expensive than that of racemic

compounds but, fortunately, racemic pheromones
In Dysmicoccus grassii, a main pest of Canary can be used because the unnatural stereoisomers
Islands banana, the principal components have no behavioral effect and, therefore, are
()-(R)-lavandulyl propionate and acetate in a benign (Zada et al. 2008). A unique case is the
6:1 ratio were identied by volatile collection pheromone of M. hirsutus; it contains a chiral
and GCMS analysis from aeration of virgin acid function that must have the correct chirality
females. (R)-lavandulyl propionate induced a for biological activity (Zhang and Amalin 2005;
stronger attractive effect when compared with Zhang et al. 2006). The passionvine mealybug is
(R)-lavandulyl acetate (de Alfonso et al. 2012). strongly inhibited by the (Z)-stereoisomer of its
Although the males of several mealybug spe- pheromone, suggesting that this compound may
cies are attracted to the females, sex pheromones be the pheromone of a related sympatric species
are yet to be identied (e.g., Phenacoccus herreni (Millar 2008). Unlike moths and beetles, which
(Cox&Williams)). are generally sensitive to isomers (structural and
chemical) of their pheromone components,
mealybugs are less sensitive to stereoisomers. In
14.7 Synthesis of Pheromones/ practice, this means that the use of mixture of iso-
Pheromone Production mers of the pheromone will be effective for con-
trolling most of the mealybug pheromones.
14.7.1 Pheromone Production Moreover, mealybugs are responsive to small
amounts (doses of about 1 mg) of the phero-
Pheromones must be isolated, identied, and mones (Millar et al. 2005b; Zhang and Amalin
synthesized before any basic or practical studies 2005; Sugie et al. 2008), so that potentially it is
can be performed. Entomologists and chemists possible to achieve pheromone-based control at
must cooperate closely in order to achieve these relatively low costs. Not all the mealybug sex
goals. Despite the availability of modern analyti- pheromones are commercially available. In fact,
cal equipment, the identication of natural most of them, except for those of the citrus
mealybug sex pheromones remains a difcult mealybug and the vine mealybug, are synthe-
and laborious task. Mealybugs are small or tiny sized only for research in small (milligram)
insects that release minute quantities of phero- quantities. The citrus mealybug pheromone, for
mone; therefore large numbers must be reared, example, which has a rather complex structure,
and often tedious separation of virgin females has been synthesized via a variety of routes, but it
must be done to collect sufcient amounts of still is not available in large quantities (hundreds
pheromone for isolation and identication. Males of grams) required for mating disruption. At
having a short lifespan of at most a few days are present, only commercial lures for monitoring
required for bioassay, either by attraction tests or are available. Because of the worldwide eco-
by GCEAG (gas chromatography electroanten- nomic importance of the mealybugs, there is a
nography). All known mealybug pheromones are need to improve the efciency of pheromone
monoterpenoid esters, mostly of simple acids. synthesis and to make the pheromone available
Unlike moth sex pheromones, the mealybug for control application. A series of analogs of this
pheromones are not homologous compounds; pheromone was prepared, in order to nd a less
their structures vary signicantly, and three types expensive attractant (Liu et al. 1995; Dunkelblum
of structures have been found so far: open chain et al. 1987), but most of them were insufciently
esters, cyclobutane derivatives, and cyclopentane attractive, except for a homologue in which a
rings. All mealybug pheromones, except the Pl. cyclobutaneethanol moiety replaced the cyclobu-
minor and Pl. kraunhiae pheromones, are chiral tanemethanol moiety in the natural pheromone.
compounds. Generally, enantioselective synthe- The homologue displayed about 40 % attractive-
sis of chiral compounds is much more compli- ness as compared with the pheromone, and in
14 Semiochemicals in Mealybugs 183

some eld tests it was as active as the latter (1R cis-3-isopropenyl-2-2-dimthyl cyclobutane
(Dunkelblum et al. 1987). The advantage of the methyl acetate) was found to attract males effec-
homolog is that its synthesis is easier and less tively (Dunkelblum et al. 1986). Alcohol analogue
expensive than that of the pheromone. Some (1R-cis)-3-isopropenyl-2-2-
pheromone analogs of the Comstock mealybug, dimethycyclobuanemethal) was an effective
Pseudococcus comstocki Kuwana, were also syn- attractant to P. citri, and homologue (1R-cis)-3-
thesized and tested in the eld (Uchida et al. isopropeny-2,2 dimethyl cyclobutane ethylacetate
1981; Bierl-Leonhardt et al. 1982). 2,6-dimethyl- at 2,000 g per dispenser was equal to 500 g
1,5-heptadien-3-yl acetate and three of its ana- pheromone (Dunkelblum et al. 1986). Analogue
logues of the sex pheromone of Pseudococcus of pheromone of P. citri, (+)-(1R)-cis-2-2-
comstocki (Kuw.), a pest of agricultural crops dimethyl-3-isopropenyl cyclobutano methanol
including apple and pear, were synthesized and acetate was synthesized using starting material cis-
evaluated for their attractiveness to males. All pinoic acid or cis-pinonic aldehyde, which were
four compounds were found to be the effective obtained from cheap -pinene and conversion of
attractants for the insect, but the synthetic sex the pinonic derivatives to pinononic derivatives
pheromone showed a two- to seven fold higher was achieved through Hundsdiecker reaction.
activity than the analogues (Uchida et al. 1981). Pinononyl aldehyde was used for synthesis of
pheromone through Wittig reaction (Dunkelblum
et al. 2002). Structural analogue of (+) cis-
14.7.2 Synthesis of Pheromones (1R)-(3)-isopropenyl-2-2-dimethyl cyclobutane
methyl acetate, the sex pheromone of P. citri, was
Through modications of acetoxy group, several synthesized and eld-tested in grapefruit orchards
pheromone analogues were synthesized for and the most active analogue was (+)-(cis-(1R)-
different species of mealybugs. A synthetic 2-(3-iso-propenyl-2-dimethyl cyclobutane ethyl
pheromone would provide a much more econom- acetate (Dunkelblum et al. 1987).
ical, convenient, and useful survey tool. Synthesis
of pheromone compounds of Pl. minor, Pl. citri, Maconellicoccus hirsutus
and Ps. viburni was done successfully (Millar The sex pheromone of M. hirsutus, Maconelliol,
2008; Ho et al. 2007; Kukovinets et al. 2006; was synthesized in steps from Alpha pinene, and
Millar and Midland 2007). the key step was the dehydration of steps 57
through the intermediate 6 (Zhang et al. 2004). Planococcus citri
The mealybug sex pheromones that have been Pseudococcus viburni
identied generally are complex molecules, An improved diastereoselective synthesis of
which are relatively difcult to synthesize on a (1R*,2R*,3S*)-1-acetoxymethyl-2,3,4,4-
large scale. Nevertheless, because male mealy- tetramethylcyclopentane 1, the sex pheromone of
bugs are so exquisitely sensitive to the phero- Pseudococcus viburni, was described and the key
mone, with lures containing only a few step was diastereoselective catalytic hydrogena-
micrograms remaining active for at least several tion of the tetrasubstituted double bond in
months under eld conditions, widespread use of 2,3,4,4-tetramethyl-cyclopent-2-enone 4 to give
pheromone-baited traps for monitoring mealy- the thermodynamically less favored cis-2,3,4,4-
bugs is economically feasible. For example, 1 g tetramethyl-cyclopentanone 3a (Zou and Millar
of racemic pheromone is sufcient to prepare 2011). The pheromone of P. viburni was also syn-
50,000 lures or more @20 g per lure. thesized from pentalactone (Hajare et al. 2010).
In Pl. citri, (1R,3R)-3-isopropenyl-2,2- In the obscure mealybug Ps. viburni,
dimethylcyclobutanemethyl acetate (C12H20O2) 2,3,4,4-tetramethylcyclopentyl)methyl acetate
was identied, and a simple synthesis path was was identied as the sex pheromone. The active
developed in Israel, and the synthesized material compound has a number of isomers, and all were
184 N. Bakthavatsalam

made to conclusively verify the identity of the traps baited with virgin females. A mixture of
insect-produced compound. An efcient synthe- stereoisomers of the pheromone compound can
sis of the active compound, capable of being be used for eld trapping without adverse effects
scaled up to produce multigram quantities, was on trap catch (Unelius et al. 2011).
then developed. The pheromone was eld-tested
in California vineyards and nurseries, and by col- Pseudococcus longispinus
laborators in South America and New Zealand. A single compound was unique to the headspace
The pheromone is extraordinarily active, with of the sexually mature female Ps. longispinus.
lures loaded with sub-milligram quantities The rst reported synthesis involves a polyphos-
remaining attractive to male mealybugs for sev- phoric acid-mediated cyclization of isobutyl
eral months. In South Africa, The sex pheromone 2-butenoate. The cyclopentenone was then con-
for P. viburni was recently identied and synthe- verted into the allylstannane after being reduced.
sized in South Africa. There was a positive and A short and efcient synthesis of the mealybug
signicant relationship between the fruit infesta- pheromone was developed from readily available
tion and number of P. viburni adult males caught iodoketone with an overall yield of 21 %. The
in pheromone-baited traps (r2 = 0.454, P < 0.001) pheromone has been shown to have extremely
in pome orchards. The action threshold level was high biological activity; in lures, just 25 g of the
estimated to be 2.5 male P. viburni caught per racemic pheromone can attract males for more
trap per fortnight at an economic threshold of 2 than 3 months (Bakonyi 2012). The synthesis
% fruit infestation. This monitoring method was of a recently identied and highly active sex
less labor-intensive, more accurate, and quicker pheromone of Ps. longispinus, was reported by
than the current visual sampling and monitoring Kurhade et al. (2013).
techniques (Mudavanhu et al. 2011). Pseudococcus comstocki Pseudococcus calceolariae The synthesis of the acetate of
Traps baited with 1001,000 g of racemic chry- 2,6-dimethylhepta-1,5-dien-3-olthe sex phero-
santhemyl 2-acetoxy-3-methylbutanoate cap- mone of the Comstock bughas been carried out
tured 420-fold more males than traps baited by condensing isobutenyl lithium with
with virgin females. In Chile, a single dose of 3,4-epoxy-2-methylbut-1-ene and acetylating
100 g was known to capture 1,171 males, the 2,6-dimethylhepta-1,5-dien-3-ol formed. The
whereas none were captured in control traps. An overall yield of pheromone was 46 % (Ishchenko
isomeric mixture of synthetic 3 proved to be et al. 1989). The synthesis of racemic versions of
highly attractive to male mealybugs in the eld in pheromones of Ps. comstocki was done through
New Zealand and in Chile. Male mealybugs were reductive lithiation of allyl phenyl thioesters
highly attracted to the racemic material and this followed by transmetallation, producing allylme-
will greatly facilitate the development of the tallics, which react selectively with carbonyl
pheromone for monitoring and control of this compounds at the most on least-substituted ter-
pest, because racemic 3 can be readily synthe- minus and the latter results in cis-olen
sized from commercially available intermediates (McCullough et al. 1991).
(El-Sayed et al. 2010). This activity of 1R,3R)-
pyl]methyl (R)-2-acetoxy-3-methylbutanoate in 14.8 Commercial Development
Pseudococcus calceolariae was further conrmed of Pheromones
by testing synthetic stereoisomers of the com-
pound as lures in traps for adult male mealybugs. Currently, of these seven pheromones, only the
Traps baited with 1,000 g of the pheromone vine mealybug Pl. cus pheromone is commer-
compound caught 36 times more males than cially available, but Millar is working to transfer
14 Semiochemicals in Mealybugs 185

the manufacturing technology to companies that Place the rubber septum containing the phero-
produce pheromone products. None of the phero- mone (lure) inside the trap on top of the sticky
mones are protected by patents; therefore, all are coating on the bottom panel.
freely available for the commercial development.
Companies also need to know that there is a sub- Trap Placement
stantial market for these products, so growers Tie the trap to the plant at 23 feet above
should communicate their needs to company rep- ground level. Traps baited with virgin
resentatives to expedite the entry of mealybug Pseudococcus comstocki females, placed in
pheromone traps into the market place. Ps. comstocki-infested fruitless mulberry
Chemist Aijun Zhang in Beltsville, MD, trees about 9 ft above ground level, had
developed the pheromone of M. hirsutus, which caught an average of 225 Ps. comstocki
mimics the female mealybugs scent, according males compared with 6 ft by each of the
to a news release. South Carolina Scientic Inc., other traps (Moreno et al. 1972). Make sure
of Columbia, SC, will market the chemical. The leaves and shoots are not obstructing the
sex pheromone, placed inside sticky traps, effec- entrance into the trap. Do not hang it too low
tively monitors and traps male mealybug. By lur- or too high in the canopy.
ing males to traps, the pheromone would provide Place the trap at the center of the block for
a much more useful detection tool. Relatively surveying the largest area possible.
high concentrations of the pheromone repel
males away from the source, disrupting mating. Labeling Traps
However, natural enemies of the mealybug are Label the trap with the block name and
not attracted to the scent, so biological control row number, where the trap was placed
would not be compromised (http://www.the- and the dates it was set out in the field and removed.
bug_ pheromone_117886474.html#sthash. Label the outer side of the trap with the fol-
2KIGfvcv.dpuf). Commercial lures of Ps. longis- lowing information: date of placement (DOP),
pinus and Ps. maritimus also became available vineyard and block name, row and vine num-
from Suterra LLC (Bend, OR) in 2010. ber, and lure (L) type. When you remove the
trap, write the date of removal (R). Use a per-
manent marker.
14.9 Traps Trap Density
Pheromone traps can attract the mealybugs Place one trap per hectare or one per smaller
within one-quarter mile from the trap site. orchard. Trapping Season

14.9.1 Trapping Guidelines Placement of traps based on the information
gathered on the seasonal activity more Trap Assembly closely in the locality. In California, place-
Obtain or purchase a red Delta trap, preferably ment of traps begins in late March to June
with a white sticky bottom panel for ease of (depending on region) and trapping is con-
viewing mealybugs. tinued through October or until the rst rain
Assemble the trap by folding in the side edges in vineyards.
to reduce the size of the openings.
186 N. Bakthavatsalam Checking Traps bugs in mulberry ecosystem (Bichina et al. 1982).

Check traps every 2 weeks for the presence of Pheromone-baited traps with larger trapping sur-
mealybugs on the sticky surface. faces (green Delta, Pherocon IIB, and Pherocon
V) captured more males of Maconellicoccus hir- Trap Replacement sutus per trap than those with smaller surfaces
Replace the trap when it becomes soiled. (Jackson and Storgard Thinline), and fewest
Lures are effective for a maximum of 8 weeks. males were captured by Storgard Thinline traps.
If no male mealybugs are found, new pheromone However, Jackson traps captured as many or
lures can be placed into old traps. Do not for- more males per square centimeter of trapping
get to re-label the new trap and note when new surface than those with larger surfaces, and the
lures are placed in the trap. time required to count males in Jackson traps was
signicantly less than in green Delta, Pherocon
IIB, and Pherocon V traps. Although all trap
14.9.2 Types of Traps designs accumulated some debris and nontarget
insects, it was rated as light to moderate for all
Multi-season plastic Delta traps are used for designs. The Jackson trap is most suitable for
monitoring and mass trapping the mealybugs. monitoring M. hirsutus populations. In addition,
These Delta traps areresistant to severe weather unlike the other traps evaluated, which must be
conditions. They are very easy to assemble and replaced entirely or inspected in the eld and
collapse at for storage. Hwang and Chu (1987a) then redeployed, only the sticky liners of Jackson
developed an effective, cylindrical, and transpar- traps require replacement, enhancing the ef-
ent plastic trap (diameter 8 cm and length 8 cm) ciency of trap servicing (Vitullo et al. 2007).
with white sticky card (8 12.5 cm) inserted at Adhesive traps, baited with virgin females of
the bottom, and traps placed at 100 cm and above Maconellicoccus hirsutus and placed on hibis-
caught more than 50 % of males. Commercially cus, captured more males than did unbaited traps
developed traps with more surface such as green (Serrano et al. 2001).
Delta, Pherocon IIB, and Pherocon V captured The color of the pheromone trap inuenced
more males than other traps (Vitullo et al. 2007). the numbers of males of Pseudococcus comstocki
Delta sticky traps, baited with 50 or 200 g of LS (Kuw.) caught. Multi-season plastic Delta traps
were used to determine the daily ight pattern are available in red and white. Generally, yellow
and the seasonal ight activity including vine traps with sticky surfaces were effective in trap-
plant infestation for P. cus (Zada et al. 2008). A ping males. Pheromone traps baited with green
method is described for handling sticky trap Delta, Pheroxin IIB, and Pherocon V trapped
cards and evaluating catches, using the sex pher- more males in Maconellicoccus hirsutus.
omones of Planococcus citri and Pseudococcus Moreover, Jackson traps captured more adults
comstocki (Fargerlund and Moreno 1974). In per square centimeter (Vitullo et al. 2007). The
USA and Japan, 2,6-dimethyl-1,5-heptadien-3-yl color preference was red = dark
acetate was identied in Ps. comstocki and a syn- green = black > green > yellow > white. According
thetic material was prepared in the Moldavian to Hwang and Chu (1987a, b), red color sticky
area of the USSR. The sticky traps proved very cards are the most attractive to the males of
successful in attracting and catching male mealy- Planococcus citri.
14 Semiochemicals in Mealybugs 187

Triangular tent-shaped Yellow trap Yellow traps

14.10 Pheromone-Based damage. Monitoring for mealybug infestation is

Management Tactics quite labor intensive as mealybugs are often
located in the protected areas of plants like bark
Sex pheromones of insects, including mealybugs, crevices and leaf axils. Pheromone traps may be
are natural compounds emitted by virgin females used as an early warning tool for grape growers
in order to attract conspecic males for mating. to monitor mealybug activity and to detect the
The sex pheromones are effective in extremely initial establishment of mealybug colonies. The
small quantities; they are nontoxic and can be traps are baited with female mealybug phero-
applied in various ways. Unlike pesticides, these mone impregnated in a rubber lure. The traps are
chemicals are species specic and do not affect placed within the vine canopy to attract winged
benecial insects. The behavioral impacts of the male mealybugs. When the mealybug population
semiochemicals are limited to the target pest is small, using a sex pheromone trap to attract
organisms. The potential of mealybug sex phero- winged males is far more efcient than trying to
mones as an alternative and ecologically friendly search vines over a large area for hidden females.
means for monitoring and control is important The male mealybugs can y about one-half mile,
and promising. Sex pheromones are used in lures and it can be wind-blown much further. Mealybug
for monitoring, for detection of outbreaks, and monitoring methods involve examination of spe-
for population management. Monitoring systems cic plant parts for live individuals, and detection
provide vital information for the timing of insec- of honeydew, sooty mold, or ant activity (Franco
ticide applications. Population levels can be et al. 2004a, b; Millar et al. 2005a). Sampling
reduced or controlled by mass trapping, mating procedures have been developed for several
disruption, or lure and kill. The success of these mealybug species and various crops, such as the
methods depends on the availability of the phero- citrus mealybug, Pl. citri (Martinez-Ferrer et al.
mone, and on an appropriate formulation and 2006), the grape mealybug, Ps. maritimus
deployment. In contrast to the extensive use of (Geiger and Daane 2001), or the sugarcane
sex pheromones in controlling beetle and moth mealybug, S. sacchari (Allsopp 1991; Debarro
pests, sex pheromones are yet to be used to a 1991). However, the cryptic occurrences of
great extent in controlling the mealybugs. mealybugs as well as their typical clumped spa-
tial distribution (Allsopp 1991; Martinez-Ferrer
et al. 2006; Nestel et al. 1995) make monitoring
14.10.1 Monitoring laborious and often impracticable. Population
estimates based on the level of male capture in
Sampling is a key element of mealybug manage- pheromone-baited traps are considered more
ment, because of the need for real-time informa- convenient (Millar et al. 2005a). Much work has
tion on the mealybug population and the potential been done to optimize these sampling methods,
188 N. Bakthavatsalam

especially in relation to trap design, trap color, Information on the level of male capture in spring
type of dispenser, pheromone dose, and bait lon- or early summer by application of pheromone
gevity and range (Francis et al. 2007; Franco traps is used to predict mealybug density or per-
et al. 2004a, 2008a, 2009; Millar et al. 2002; centage of fruit infestation and consequently to
Vitullo et al. 2007; Walton et al. 2004; Zada et al. assist in the decision making for the purpose of
2004, 2008). Nevertheless, the use of pheromone the citrus mealybug management (Franco et al.
traps as a monitoring tool for mealybug damage 2001). The analogous compound, 1R cis-3-
risk assessment depends on the existence of a isopropyl-2-2-diemthyl cyclobutyl methyl acetate
reasonable relationship between the number of was impregnated at 2,000 g in each dispenser
males captured in pheromone-baited traps and almost equaling 500 g of pheromone of Pl. citri
other mealybug infestation parameters, as to monitor the mealybugs (Franco et al. 2004b). In
recorded by other means, usually, visual sam- Mediterranean Basin, the best time for releasing
pling. A linear relationship was found to exist the natural enemies Cryptolaemus montrouzieri
between the vine mealybug, Pl. cus (Walton Muls. and Leptomastix dactylopii How. for the
et al. 2004), and the citrus mealybug, Pl. citri control of Pl. citri in citrus orchards was deduced
(Franco et al. 2001). However, this correlation from mealybug population monitoring by means
may be affected by different factors, including of traps containing the sex pheromone of P. citri
the weather, the activity of natural enemies, and (Panis 1981).
the phenological gap between male captures and
infestation level (Franco et al. 2001, 2008a). Pseudococcus longispinus
and Pseudococcus viburni Pseudococcus comstocki Positive and signicant relationship exists
The seasonal ight activity of Ps. comstocki in between pome fruit infestation and number of Ps.
California was monitored with sex pheromone vulbuni in pheromone traps baited with phero-
traps (Meyerdirk and Newell 1979). In the mone, and pheromone monitoring was done to
Moldavian area of the USSR, a synthetic material estimate the action threshold, which was esti-
of sex pheromone proved very successful in mated to be 2.5 male Ps. viburni (Mudavanhu
detecting not only the presence of Ps. comstocki et al. 2011). Lures containing 25 g per lure was
but also the information on its population density attractive to Ps. viburni and Ps. longispinus.
in mulberry ecosystem (Bichina et al. 1982). Racemic mixtures of S-lavandulyl senecioate and
Pheromone of Ps. comstocki containing (S)-lavandulyl isovalerate recorded good capture
2,6,-dimethyl-1,5,-heptadient at the rate of 200 (Zada et al. 2008). Operational parameters of
g per trap, placed at a height of 1.52 m, was able traps baited with the pheromones of three
to trap the adult males, and used for recording the mealybug species were optimized in nurseries
uctuation of daily and seasonal ight dynamics producing ornamental plants. All pheromone
(Smetnik and Rozinskaya 1988). doses (1320 g) attracted Ps. longispinus and
Ps. viburni males, with the lowest dose (1 g) Planococcus citri attracting the fewest males for both species.
Monitoring population densities of Planococcus Lures containing 25-g doses of either phero-
citri in citrus ecosystem was based on male mone had effective eld lifetimes of at least 12
capture using traps baited with female sex phero- weeks. Pheromone traps were used to detect
mones. Pheromone of Pl. citri was used for the infestations of Ps. longispinus throughout the
early detection of the pest occurrence in citrus season and to track population cycles. When
elds (Ortu and Delrio 1982). In Israel, the sea- pheromone-baited traps for Ps. longispinus were
sonal population uctuations and trends of Pl. compared with manual sampling, trap counts of
citri were monitored (Hefetz and Tauber 1990; male mealybugs were signicantly correlated
Tauber et al. 1985) and traps were being used in with mealybugs counted on plants in the vicinity
conjunction with biological control methods. of the traps (Waterworth et al. 2011).
14 Semiochemicals in Mealybugs 189 Planococcus cus 14.11 Mixed Mealybugs

Vine mealybug Pl. cus pheromones are placed
in traps and used to deduct the infestation of Often in eld conditions, more than one mealy-
mealybugs. Typically, they are effective in bug species complex exist, necessitating the use
detecting new infestations. A sex pheromone of blend of more than one pheromone for trap-
produced by female mealybugs is used inside ping multiple species. The same generic lure can
each trap to attract adult males nearby. The males attract three species of mealybugs, which would
enter seeking the females and become trapped cut costs for growers by allowing them to deploy
inside. Although they may be designed in differ- a single pheromone trap rather than three. Lures
ent shapes, tent-shaped red traps are recom- loaded with a mixture of the pheromones of Ps.
mended. In eld trials conducted by Millar et al. longispinus, Ps. viburni, and Pl. citri were as
(2002), it was observed that the rubber septa attractive to Ps. viburni and Ps. citri as lures with
loaded with 100 g of racemic pheromone was their individual pheromones. Response of Ps.
able to effectively capture the males of Pl. cus longispinus to the blend was decreased by 38 %
for a period up to 12 weeks, and Delta traps were compared with its pheromone as a single compo-
more effective than double-sided adhesive sticky nent. This should not affect the overall efcacy
cards (Millar et al. 2002). of using these lures for monitoring the presence
of all three mealybug species simultaneously Maconellicoccus hirsutus (Waterworth et al. 2011). Trapping indicated a
The pheromone was used to attract the males of sharp peak in male citrophilus mealybug ight
Maconellicoccus hirsutus (Vitullo et al. 2007). activity in mid-February with a gradual decline
Laboratory-prepared (R)-lavandulyl (S)-2- thereafter. Long-tailed mealybug ight activity
methylbutanoate and (R)-maconelliyl (S)-2- increased during March and peaked in late April
methylbutanoate blended in a ratio of 1:5 on when trapping ceased. Higher numbers of
rubber septa impregnated with a dose of 110 g citrophilus mealybug males (36,764) were
were attractive to males of M. hirusutus for a trapped than long-tailed mealybug (693).The
period of 21 weeks (Zhang and Amalin 2005). It dominant species was the longtailed mealybug,
was found that the mixture of lavandulyl and identied on 92 % of infested fruit. Citrophilus
maconellyl in a 1:5 ratio signicantly attracted and obscure mealybugs (Ps. viburni) were identi-
more males of M. hirsutus and was used to track ed on 3 % and 5 % of infested fruit, respectively
the geographical dispersal of the species (Shaw and Wallis 2011).
(Gonzalez-Gaona et al. 2010). Phenacoccus madeirensis 14.11.1 Mating Disruption

The pheromones trans-1R,3R-chrysanthemyl
R-2-methylbutanoate and R-lanadulyl R-2- Mating disruption seems to be more advanta-
methylbutanaoate have shown the effectiveness geous in mealybugs than in Lepidoptera as
in attracting males of P. madeirensis (Ho et al. mealybug females are sessile and cannot migrate
2011). from one area to another as moths do. On the
other hand, mating disruption of mealybug pests Pseudococcus viburni presents problems, especially because the com-
Pheromone-baited traps have been used in New plex structure of the pheromones prevents large-
Zealand to detect Ps. viburni in apple orchards scale synthesis. The vine mealybug pheromone is
(Bell et al. 2005). the only mealybug pheromone that can readily be
190 N. Bakthavatsalam

synthesized in one step from two commercial ping, but not signicant enough to cause any
starting materials, so that it can be prepared in reduction in the infestation on fruits in
large quantities, sufcient for eld work, includ- Mediterranean countries (Franco et al. 2003).
ing mating disruption (Ujita and Saeki 2008; Similarly in Israel and Portugal, signicant
Walton et al. 2006). When the pheromone was reduction of male numbers can be achieved by
applied to the leaves as a sprayable microcapsule mass trapping with sticky plate traps (30 cm 30
formulation, crop damage was reduced from 9 to cm) baited with 200 g of pheromone used at a
11 % in control plots to 34 % in treated plots; rate of one per citrus tree, although fruit infesta-
however, the effective life of the formulation tion did not reduce signicantly. Therefore, as
presents a technical problem that needs to be the pheromone trapping system used cannot
solved. The efciency of the pheromone formu- reduce the number of attracted males effectively,
lation in the eld declined after 3 weeks, indicat- it is most likely that many of them originated
ing that more than four applications per season from outside the subplot. In fact, males are
were needed. The proximity of the mealybug attracted to the pheromone source from ranges up
sexes on emergence may also impair the success to at least 100 m (Branco et al. 2006; Franco et al.
of mating disruption (Walton et al. 2006). Mating 2004a). On the other hand, the higher level of
disruption in Planococcus kraunhiae through the mating observed in mass-trapping plots early in
use of pheromone, 2-isopropyliden-5-methyl-4- the spring, when the mealybug density is usually
hexenyl butyrate controlled the mealybug popu- very low, suggested that mass trapping led to a
lations in the eld in Japan (Teshiba et al. 2009). strong attraction of males from outside the sub-
There was a lesser density of Planococcus cus plots. In light of this nding, it was postulated
on leaves of vines treated with plastic dispensers that early in the season, when the male popula-
with 100 mg each of synthetic sex pheromone tion is usually low, the attraction of males to the
than the control; however, the difference was not edge of the orchard by using attractannihilate
signicant (Cocco et al. 2011). Due to its effec- tactics combined creates a male vacuum inside
tiveness in traps, developing the pheromone to the plot and, consequently, reduces mating and
control vine mealybug populations (Planococcus infestation (Franco et al. 2004a).
cus) using mating disruption was pursued
(http:// advancinggreenchemistry. org/ catch-all/ Maconellicoccus hirsutus
mating-disruption-as-a-pest-management-tool- The quantum of pheromones produced through
in-californias-wine-industry/). synthesis was not sufcient to use for mass
trapping and mating disruption. However
recently, Chemist Aijun Zhang in Beltsville, MD,
14.11.2 Mass Trapping developed the pheromone, which mimics the
female mealybugs scent, and South Carolina
An articial lure might also enable the development Scientic Inc., of Columbia, SC, will market the
of mass trapping and mating disruption technology chemical. There is also a second potential control
for managing this pest, which would complement strategy (
the ongoing biological control eradication efforts. market pink mealybug pheromone_117886474.
In addition to their use for detection and monitoring html#sthash.2KIGfvcv.dpuf).
of insect populations, pheromones also have a
potential use in insect control, for example, by Pseudococcus calceolariae
mating disruption or attract-and-kill technologies. In 1975, a mass-trapping experiment was carried
out against Pseudococcus calceolariae (Mask.), Planococcus citri which was causing heavy damage on citrus near
Pheromones are yet to be exploited to a great Salerno, Italy; 79 traps baited with 1,538 virgin
extent for mass trapping of mealybugs. There females were placed in 25 orange trees over an
was a signicant reduction in the population of P. area of 1 ha in a single orchard, and they caught
citri when pheromone was used for mass trap- about 300,000 males of the species. Populations
14 Semiochemicals in Mealybugs 191

were sampled in 19751978 in order to assess the The sex pheromone of mealybugs may be
long-term effect of the traps on population used by their natural enemies as a kairomonal cue
dynamics. Up to 1976, a sevenfold reduction in in host or prey selection. Anagyrus pseudococci
captures of males and a tenfold decrease in popu- sp.n. is an effective parasitoid of vine mealybug
lations on fruits in this orchard were registered. Pl. cus and citrus mealybug Pl. citri. Anagyrus
Flight peaks of Ps. calceolariae occurred in mid- pseudococci in California vineyards was attracted
May, mid-July, and late September. It was not to the pheromone ((+)-lavandulyl senecioate
possible to determine from the experiments (LS)) of Pl. cus (Millar et al. 2002; Franco et al.
whether the decline in Ps. calceolariae was due 2008c) but Anagyrus pseudococci sp.n. was not
to either the earlier catches of males in the traps attracted to the pheromone ((+)-(1R,3R)-cis-2,2-
or sudden increases in populations of coccinellid dimethyl- 3-isopropenyl-cyclobutanemethanol
predator (Rotundo et al. 1979a, b). acetate (PcA, namely, planococcyl acetate) of P.
citri (Franco et al. 2008c, 2011; da Silva et al. Planococcus cus 2009a, b); and this kairomonal response was an
The use of synthetic sex pheromones, such as innate behavior trait. An interesting aspect of this
those found in Suterras CheckMate products program is that a parasitoid of the vine mealybug
for mating disruption of vine mealybug, aims to (Anagyrus pseudococci) may be attracted to the
prevent adult males from mating. The use of mealybug pheromone as a host-nding cue,
degree-day models, pheromone traps, and eld resulting in greater levels of biological control.
observations are helpful for detecting the earliest There is a minimal risk of parasitoids being
colonies of mealybugs. By preventing mating caught if lures are deployed in triangular tent-
and subsequent egg laying, vine mealybug popu- shaped Delta traps. It was also found that the
lations can be dramatically reduced to below presence of Pl. cus sex pheromone signicantly
economically damaging levels. increases the parasitization rate of Pl. citri colo-
nies by Anagyrus pseudococci. (Franco et al.
2008b). In eld trials in Portugal, Italy, and
14.11.3 Kairomonal Response Israel, the rate of parasitism by A. pseudococci
was improved through the use of pheromone
The pheromone-lled air also acts as kairomones (Franco et al. 2001). In Sicilian orchards (Italy)
for several predators and parasitoids. The sex infested with Pl. cus, the number of captured A.
pheromone emitted by mealybug virgin females pseudococci females per trap was signicantly
provides reliable information on the location of a higher in LS (sex pheromone (S)-(+)-lavandulyl
potential host for mealybug parasitoids, because senecioate (LS)-baited traps resulting in the
of the sedentary nature of mealybugs. enhancement of the parasitoid performance
Furthermore, because of the typical clumped spa- (Mansour et al. 2010).
tial pattern of mealybugs, the sex pheromone will Pheromone-based mating disruption of vine
also be a convenient chemical cue by which the mealybug indicated that the treatment had no
parasitoid can efciently locate aggregates (colo- negative effect on the level of parasitization
nies) of hosts, which are expected to emit a stron- (Walton et al. 2006) with Pl. cus by A. pseudo-
ger pheromonal signal than that of single virgin cocci. The kairomonal response of Anagyrus
females (functional response). Thus, sex phero- pseudococci sp.n. could be explored in connec-
mones of mealybugs could serve as a novel and tion with biological control tactics, by enhancing
efcient tool to support the classical biological parasitization of Pl. citri as a component of inte-
control of invasive mealybug species, by identi- grated pest management strategies, by means of a
fying, in the region of origin of the target species, similar approach to that used against aphid pests
parasitoids that could be the potential candidates (Powell and Pickett 2003). Rotundo and
for use in the biological control program (Franco Tremblay (1975) reported that traps baited with
et al. 2008c). virgin females of Ps. calceolariae captured sig-
192 N. Bakthavatsalam

nicant numbers of the encyrtid Tetracnemoidea (Pseudococcus calceolariae) sex pheromone

peregrinus (Compere) (=Tetracnemoidea traps that were being monitored at heavily
peregrina(Compere); Arhopoideus peregrinus). infested mealybug orchards. It is quite conceiv-
A kairomonal response of the encyrtid able that the high numbers of parasitoids in pher-
Pseudaphycus maculipennis Mercet to the sex omone traps and the low numbers of citrophilus
pheromone of the obscure mealybug, Ps. Viburni, mealybugs in fruit at harvest indicated that it was
was also observed in eld experiments with pher- an effective biological control agent in these
omone traps (Bell et al. 2008). Two species of properties (Shaw et al. 2012).
mealybug parasitoids were caught in traps baited
with the sex pheromone of Ps. cryptus in a citrus
orchard in Japan (Arai 2002). Cassava plants 14.12 Dogs for Monitoring
infested with the mealybugs are attractive to the Mealybug Incidence
parasitoids such as Aenasius vexans Kerrich,
Apoanagurus diversicornis, and Acerophagus Dogs have been trained to detect the presence of
coccois Smith. A compound O-caffeoylserine is females of grapevine mealybugs in California.
attractive to the parasitoids of mealybugs The 3-month-old puppies of Golden retriever
(Calatayud et al. 2001). have been frequently exposed to the pheromone
In New Zealand, Acerophagus maculipennis, component of grapevine mealybugs and when
a recently introduced biocontrol agent, has been they are around 2 years old, they are fully trained
recorded from sex pheromone traps of its target to identify the presence of mealybugs. The dogs
host, obscure mealybug (Pseudococcus viburni). are capable of identifying even the twigs with the
Alamella mira Noyes, an accidentally introduced females. This method of using dogs olfactory
parasitoid in New Zealand, was captured on senses has resulted in saving of crops worth sev-
sticky bases in citrophilus mealybug eral millions besides saving the environment.

Dog squad strategies being considered to stop the vine mealybug

14 Semiochemicals in Mealybugs 193

14.13 Future Prospects semiochemicals for the complex pheromone

species in any crop will be advantageous to
The pheromones for only a few of species the farmers and such generic pheromone or
such as Planococcus citri and M. hirsutus semiochemical will also be of commercial
were isolated, identied, and used in other success for the entrepreneurs.
countries. Use of these pheromones as a moni- For the effective management of mealybug,
toring tool will be a great boon for the farmers mating disruption and inoculative releases of
to identify the initial stages of infestation. parasitoids (such as Anagyrus pseudococci)
However, the pheromone for several impor- were considered as effective strategies for the
tant invasive species such as Paracoccus mar- management of mealybugs in vineyards
ginatus Williams and Granara de Willink and (Daane et al. 2008). This will enable environ-
Phenococcus solenopsis Tinsley needs to be mental friendly, healthy, and safe methods of
identied for eld monitoring. Besides moni- mealybug management of the future.
toring the incidence, the pheromone may also In India, the pheromones were seldom used
be used to study the spread of the mealybug, though pheromones for several Indian species
for example, the dispersal pattern of P. mar- have been identied elsewhere. A concerted
ginatus and Pseudococcus jackberdsleyi effort is needed to use pheromones for
Gimpel and Miller can be easily documented monitoring and for mating disruption of the
in time and space. mealybug species by the plant protection
There are several species of potential inva- experts. The entrepreneurs should take efforts
sives such as Phenacoccus manihoti, and the either to import the pheromone or to develop
identication of pheromones for these species facilities for indigenously synthesizing the
will enable us to monitor the entry of this spe- pheromones and market at a cheaper rate in
cies into India. It will be worthwhile to isolate, order to guarantee the continuous availability
identify, and synthesize these pheromones for of pheromones to the farmers.
the quarantine monitoring throughout the Wherever the pheromones were not identied
world. Installations at ports, airports, and for the species, both indigenous and exotic,
other entry points will enable in the early efforts must be made to identify and synthesize
detection of these mealybugs. pheromones that can be useful for monitoring
The technique for the isolation, identication, the pests, which can be effective tools for quar-
and characterization of mealybug pheromones antine monitoring and population studies.
has been standardized over the years, enabling Awareness should be brought to the farmers
us to identify the pheromones for any species. and the pest management experts on the scope
Moreover, the synthesis of pheromones for a of using the pheromones for effective man-
few species has been accomplished. However, agement of mealybugs.
the ability to synthesize pheromone on a large Work has to be initiated on the role of plant
scale remains an unfullled task resulting in volatiles in the attraction of mealybugs and
the use of pheromone only for monitoring, their natural enemies, which can be used both
and not for the mating disruption and mass for monitoring of pest and natural enemies
trapping. Efforts are needed to develop shorter and for reinforcing the natural enemy
synthesis schemes for the effective synthesis populations.
of pheromones in both quality and quantity. Collaborative efforts between countries need
Often the infestation of complex species of to be made through international funding to
mealybugs was encountered in many crops, isolate, identify, and synthesize pheromones
thus necessitating the identication and use of of potential invasives for quarantine screen-
generic pheromones. Generic pheromone or ing, a prophylactic measure of biosecurity.
194 N. Bakthavatsalam

References Calatayud PA, Auger J, Thibout E, Rousset S, Caicedo

AM, Calatayud S, Buschmann H, Guillaud J, Mandon
N, Bellotti AC (2001) Identication and synthesis of a
A SA (1968) Morphology and taxonomy of the adult
kairomone mediating host location by two parasitoid
males of the families Pseudococcidae and Eriococcidae
species of the cassava mealybug Phenacoccus herreni.
(Homoptera: Coccoidea). Bull Brit Mus (Nat Hist)
J Chem Ecol 27:22032217
Entomol 13(Suppl):1210
Carlsen PHJ, Odden W (1984) Synthesis of the female sex
Ahmad R, Ghani MA (1970) A note on the rearing of
pheromone of the citrus mealybug, Planoccus citri
scale insects and mealybugs on potato tubers and
(Risso). Acta Chem Scand B 38:501504
cucurbit fruits. Technical Bulletin, Commonwealth
Chacko MJ, Bhat PK, Rao LVA, Deepak Singh MB,
Institute of Biological Control, 13, pp 105107
Ramanarayan BP, Sreedharan K (1978) The use of the
Allsopp PG (1991) Binomial sequential sampling of adult
lady bird beetle Cryptolaemus montrouzieri for the
Saccharicoccus sacchari on sugarcane. Entomol Exp
control of coffee mealybugs. J Coff Res 9:1419
Appl 60:213218
Chibiryaev A, Rukavishnikov AV, Tkachev AV, Volodarskii
Arai T (2002) Attractiveness of sex pheromone of
LB (1991) New synthesis of the sex pheromone of the
Pseudococcus cryptus Hempel (Homoptera:
mealybug Planococcus citri from a -pinene. Zh Org
Pseudococcidae) to adult males in a citrus orchard.
Khim 27:12091213
Appl Entomol Zool 37:6972
Cocco A, Coinu M, Lentini A, Serra G, Delrio G (2011)
Arai T, Sugie H, Hiradate S, Kuwahara S, Itagaki N,
Mating disruption eld trials to control the vine
Nakahata T (2003) Identication of a sex pheromone
mealybug Planococcus cus. IOBC/WPRS Bull
component of Pseudococcus cryptus. J Chem Ecol
da Silva EB, Fortuna T, Franco JC, Campos L, Branco M,
Baeckstroem P, Li L (1990) A one pot procedure for the
Zada A, Mendel Z (2009a) Does the parasitoid
deoxygenation of , -unsaturated ketones and a syn-
Anagyrus pseudococci respond to the sex pheromone
thesis of the mealybug pheromone. Synth Commun
of major host-mealybug species? IOBC/WPRS Bull
Baeckstrom P, Bjorkling F, Hogberg HE, Norin T (1984)
da Silva EB, Fortuna T, Franco JC, Campos L, Branco M,
Cross-coupling of vinyl cuprates and allylic halides
Zada A, Mendel Z (2009b) Kairomonal response of a
and synthesis of the Comstock mealybug pheromone
parasitic wasp to the sex pheromone of the vineyard
via photooxidation of 2,6-dimethyl-2,5-heptadiene.
mealybug. IOBC/WPRS Bull 41:7982
Acta Chem Scand B 38:779782
da Silva EB, Mouco J, Antunes R, Mendel Z, Franco JC
Bakonyi JM (2012) Improved synthesis of the longtailed
(2009c) Mate location and sexual maturity of adult
mealybug pheromone. Masters theses, Paper 231.
male mealybugs: narrow window of opportunity in a
short lifetime. IOBC/WPRS Bull 41:39
Bell VA, Walker JTS, Shaw PW, Wallis RD, Suckling
Daane KM, Bentley WJ, Millar JC, Walton VM, Cooper
DM, Millar JG (2005) Mealybug monitoring and the
ML, Biscay P, Yokota GY (2008) Integrated manage-
use of sex pheromone in Hawkes Bay & Nelson apple
ment of mealybugs in California vineyards. Acta
orchards. HoRt Res internal report no 17359, 12 pp
Hortic 785:235252
Bell VA, Suckling DM, Walker JTS, Millar JG, Manning
Daane KM, Middleton MC, Sforza R, Cooper ML, Walton
LA, El-Sayed AM (2008) Obscure mealybug phero-
VA, Walsh DB, Zaviezo T, Almeida PP (2011)
mone is the kairomone of an introduced parasitoid in
Development of a multiplex PCR for identication of
New Zealand. In: Proceedings of XXIII international
vineyard mealybugs. Mol Ecol Evol
congress on entomology, 612 July 2008, Durban
(Abstract). Available at
de Alfonso I, Hernandez E, Velazquez Y, Navarro I, Primo
J (2012) Identication of the sex pheromone of the
Bichina TI, Kovalev BG, Smetnik AI, Vaganova LD
mealybug Dysmicoccus grassii Leonardi. J Agric
(1982) A test of the pheromone of the Comstock
Food Chem 60(48):1195911964
mealybug [Russian]. Zashchita Rastenii 10:46
Debarro PJ (1991) Sampling strategies for above and
Bierl-Leonhardt BA, Moreno DS, Schwarz M, Fargerlund J,
below ground populations of Saccharicoccus sacchari
Plimmer JR (1981) Isolation, identication and synthe-
(Cockerell) (Hemiptera, Pseudococcidae) on sugar-
sis of the sex pheromone of the citrus mealybug,
cane. J Aust Entomol Soc 30:1920
Planococcus citri (Risso). Tetrahedron Lett 22:389392
Doane CC (1966) Evidence for a sex attractant in females
Bierl-Leonhardt BA, Moreno DS, Schwarz M, Forster
of the red pine scale. J Econ Entomol 59:15391540
HS, Plimmer JR, DeVilbiss ED (1982) Isolation, iden-
Duelli P (1985) A new functional interpretation of the
tication, synthesis, and bioassay of the pheromone of
visual system of male scale insects (Coccida,
the comstock mealybug and some analogs. J Chem
Homoptera). Experientia 41:1036
Ecol 8:689699
Dunkelblum E (1999) Scale insects. In: Hardie J, Minks
Branco M, Jactel H, Franco JC, Mendel Z (2006)
AK (eds) Pheromones of non-lepidopteran insects.
Modelling response of insect trap captures to phero-
CAB International, Oxon, UK, pp 251276
mone dose. Ecol Model 197:247257
14 Semiochemicals in Mealybugs 195

Dunkelblum E, Ben-Don Y, Goldschmidt Z, Wolk JL, May vine mealybug sex pheromone improve the
Somekh L (1986) Synthesis and eld bioassay of the biological control of the citrus mealybug? IOBC/
sex pheromone and some analogues of the citrus mea- WPRS Bull 38:9498
lubug Planococcus citri (Risso). Bollatino de- Franco JC, Silva EB, Cortegano E, Campos L, Branco M,
laboratorio di Entomologia Agraia Filippo Silvestri Zada A, Mendel Z (2008c) Kairomonal response of
43(Suppl):149154 the parasitoid Anagyrus spec. nov near pseudococci to
Dunkelblum E, Ben-Don Y, Goldschmidt Z, Wolk JL, the sex pheromone of the vine mealybug. Entomol
Somekh L (1987) Synthesis and eld bioassay of some Exp Appl 126:122130
analogs of sex pheromone of citrus mealybug, Franco JC, Zada A, Mendel Z (2009) Novel approaches for
Planococcus citri (Risso). J Chem Ecol 13:863871 the management of mealybug pests. In: Ishaaya I,
Dunkelblum E, Zada A, Gross S, Fraistat P, Mendel Z Horowitz AR (eds) Biorational control of arthropod pests.
(2002) Sex pheromone and analogues of the citrus Springer Science + Business Media B.V., Dordrecht,
mealybug, Planococcus citri: synthesis and biological pp 233278. doi: 10.1007/978-90-481-2316-2_10
activity. IOBC WPRS Bull 25:19 Franco JC, da Silva EB, Fortuna T, Cortegano E, Branco
El-Sayed AM, Unelius RC, Twidle A, Mitchell V, Manning M, Suma P, La Torre I, Russo A, Elyahu M, Protasov
LA, Cole L, Suckling DM, Flores MF, Zaviezo T, A, Levi-Zada A, Mendel Z (2011) Vine mealybug sex
Bergmann J (2010) Chrysanthemyl pheromone increases citrus mealybug parasitism by
2-acetoxy-3-methylbutanoate: the sex pheromone of Anagyrus sp. near pseudococci (Girault). Biol Control
the citrophilous mealybug, Pseudococcus calceolar- 58(3):230238
iae. Tetrahedron Lett 51:10751078 Geiger CA, Daane KM (2001) Seasonal movement and distri-
Fall Y, Vanbac N, Langlois Y (1986) Synthesis of the pher- bution of the grape mealybug (Homoptera:
omone of the Comstock mealybug via a sila-cope Pseudococcidae): developing a sampling program for San
elimination. Tetrahedron Lett 27:36113614 Joaquin Valley vineyards. J Econ Entomol 94:291301
Fargerlund J, Moreno DS (1974) A method of handling Gonzalez-Gaona E, Sanchez-Martinez G, Zhang A,
card traps in mealybug, scale surveys. Citrograph Lozano-Gutierrez J, Carmona-Sosa F (2010)
60(1):2628 Validation of two pheromonal compounds for moni-
Figadere BA, McElfresh JS, Borchardt D, Daane KM, toring pink hibiscus mealybug in Mexico. Agrociencia
Bentley W, Miller JG (2007) Trans a-necrodyl isobutyrate, (Montecillo) 44(1):6573
the sex pheromones of the grape mealybug Pseudococcus Gullan PJ, Kosztarab M (1997) Adaptations in scale
maritimus. Tetrahedron Lett 48:84348437 insects. Annu Rev Entomol 42:2350
Francis A, Bloem KA, Roda AL, Lapointe SL, Zhang A, Hajare AK, Datrange LS, Vyas S, Bhuniya D, Reddy DS
Onokpise O (2007) Development of trapping methods (2010) Enantiospecic synthesis of sex pheromone of
with a synthetic sex pheromone of the pink hibiscus the obscure mealybug from pantolactone via tandem
mealybug, Maconellicoccus hirsutus (Hemiptera: conjugate addition/cyclization. Tetrahedron Lett
Pseudococcidae). Flor Entomol 90:440446 51(40):52915293
Franco JC, Russo A, Suma P, Silva EB, Dunkelblum E, Hashimoto K, Morita A, Kuwahara S (2008)
Mendel Z (2001) Monitoring stratagies for the citrus Enantioselective synthesis of a mealybug pheromone
mealybug in citrus orchards. Bolletino di Zoologia with an irregular monoterpenoid skeleton. J Org Chem
Agraria e di Bachicotura 33(3):297303 73:69136915
Franco JC, Suma P, Silva ED, Mendel Z (2003) Hefetz A, Tauber O (1990) Male response to the synthetic
Management strategies of mealybug pests of citrus in sex pheromone of Planococcus citri (Risso) (Hom.:
Mediterranean countries. Bull OILB/SROP 26(6):137 Diaspidae) and its application for population monitor-
Franco JC, Gross S, Silva EB, Suma P, Russo A, Mendel ing. J Appl Entomol 109:502506
Z (2004a) Is mass-trapping a feasible management Hinkens DM, McElfresh JS, Millar JG (2001)
tactic of the citrus mealybug in citrus orchards? An Identication and synthesis of the sex pheromone of
Inst Sup Agron 49:353367 the vine mealybug, Planococcus cus. Tetrahedron
Franco JC, Suma P, Silva ED, Blumberg D, Mendel Z Lett 42:16191622
(2004b) Management strategies of mealybug pests of Ho HY, Hung CC, Chuang TH, Wang WL (2007)
citrus in Mediterranean countries. Phytoparasitica Identication and synthesis of the sex pheromone of
32(5):507522 the passionvine mealybug, Planococcus minor
Franco JC, Antunes R, Lemos R, Pinto A, Campos L, Silva (Maskell). J Chem Ecol 33:19861996
EB, Branco M, Mendel Z (2008a) Do mealybug males Ho HY, Su YT, Ko CH, Tsai MY (2009) Identication and
respond to visual cues when approaching pheromone synthesis of the sex pheromone of the Madeira mealy-
sources? In: Branco M, Franco JC, Hodgson CJ (eds) bug, Phenacoccus madeirensis Green. J Chem Ecol
Proceedings of the XI International Symposium Scale 35:724732
Insect Studies, Oeiras, Portugal, 2427 September Ho HY, Ko CH, Cheng CC, Su YT, Someshwar P (2011)
2007. ISA Press, Oeiras, Portugal, pp 230231 Chirality and bioactivity of the sex pheromone of
Franco JC, Fortuna T, Silva EB, Da Suma P, Russo A, Madeira mealybug (Hemiptera: Pseudococcidae).
Campos L, Branco M, Zada A, Mendel Z (2008b) J Econ Entomol 104(3):823826
196 N. Bakthavatsalam

Hwang JS, Chu YI (1987a) The development of sex pher- male mealybug. In: Branco M, Franco JC, Hodgson CJ
omone traps for the citrus mealybug, Planococcus (eds) Proceedings of the XI International Symposium
citri (Risso). Plant Prot Bull (Taiwan) 29(3):297305 Scale Insect Studies, Oeiras, Portugal, 2427
Hwang JS, Chu YI (1987b) A bioassay method of the sex September 2007. ISA Press, Oeiras, Portugal, p 121
pheromone of the citrus mealybug, Planococcus Mendel Z, Jasrotia P, Protasov A, Kol-Maimon H, Zada AL,
citri (Risso). [Chinese]. Plant Prot Bull (Taiwan) Franco JC (2012) Responses of second-instar male
29(3):307319 nymphs of four mealybug species (Hemiptera:
Ishchenko RI, Veselovskii VV, Moiseenkov AM, Cheskis Pseudococcidae) to conspecic and heterospecic
BA, Kovalev BG (1989) Synthesis of the racemic sex female sex pheromones. J Insect Behav 25(5):504513
pheromone of Pseudococcus comstocki. Chem Nat Meyerdirk DE, Newell IM (1979) Seasonal development
Comp 25:118119 and ight activity of Pseudococcus comstocki in
Joshi MD, Butani PG, Patel VN, Jeyakumar P (2010) California. Ann Entomol Soc Am 72(4):492494
Cotton mealybug, Phenacoccus solenopsis Tinsley Millar JG (2008) Stereospecic synthesis of the sex pher-
A review. Agric Rev 31:113119 omone of the passionvine mealybug, Planococcus
Kang SK, Park CS (1990) A synthesis of ()-3-acetoxy- minor. Tetrahedron Lett 49(2):315317
2,6-dimethyl-1,5-heptadiene, the sex pheromone of the Millar JG, Midland SL (2007) Synthesis of the sex phero-
Comstock mealybug. Org Prep Proced Int 22:627629 mone of the obscure mealybug, the rst example of a
Kol-Maimon H, Levi-Zada A, Franco JC, Dunkelblum E, new class of monoterpenoids. Tetrahedron Lett
Protasov A, Eliyaho M, Mendelb Z (2010) Male 48(36):63776379
behaviors reveal multiple pherotypes within vine Millar JG, Daane KM, McElfresh JS, Moreira JA,
mealybug Planococcus cus (Signoret) (Hemiptera; Malakar-Kuenen R, Guillen M, Bentley WJ (2002)
Pseudococcidae) populations. Naturwissenschaften Development and optimization of methods for using
97(12):10471057 sex pheromone for monitoring the mealybug
Kukovinets OS, Zvereva TI, Kesradze VG, Galin FZ, Planococcus cus (Homoptera: Pseudococcidae) in
Frolova LL, Kuchin AV, Sprikhin LV, Abdullin MI California vineyards. J Econ Entomol 95:706714
(2006) Novel synthesis of Planococcus citri phero- Millar JG, Daane KM, McElfresh JS, Moreira JA, Bentley
mone. Chem Nat Comp 42(2):216218 WJ (2005a) Chemistry and applications of mealybug
Kurhade SE, Siddiah V, Bhumiya D, Reddy DS (2013) sex pheromones. In: Petroski RJ, Tellez MR, Behle
Synthesis of a sex pheromone of the long tailed mealy- RW (eds) Semiochemicals in pest and weed control.
bug, Pseudococcus longispinus. Synthesis 45:16891692 American Chemical Society, Washington, DC
Larcheveque M, Petit Y (1989) Preparation of enantio- Millar JG, Midland SL, Mcelfresh S, Daane KM (2005b)
merically pure -hydroxy esters and -hydroxy alde- (1R,2R,3S)-(2,3,4,4-tetramethylcyclopentyl) methyl
hydes. Application to the enantiospecic synthesis of acetate, a sex pheromone from the obscure mealybug:
the sex pheromone of the mealybug Pseudococcus rst example of a new structural class of monoter-
comstocki. Bull Soc Chim Fr 1:130139 penes. J Chem Ecol 31:29993005
Liu F, Li W, Wang Y, Lin J (1995) Convenient syntheses of Millar JG, Moreira JA, McElfresh JS, Daane KM, Freund
some analogs of the sex pheromone of citrus mealy- AS (2009) Sex pheromone of the longtailed mealy-
bug, Planococcus citri (Risso). Synth Commun bug: a new class of monoterpene structure. Org Lett
25:38373843 11:26832685
Mansour R, Suma P, Mazzeo G, Buonocore E, Lebdi KG, Moreno DS, Reed DK, Shaw JG, Newell I (1972) Sex lure sur-
Russo A (2010) Using a kairomone based attracting vey trap for Comstock mealybug. Citrograph 58(2):43, 68
system to enhance biological control of mealybugs Moreno DS, Fargerlund J, Ewart WH (1984) Citrus
(Hemiptera: Pseudococcidae) by Anagyrus sp. near mealybug (Homoptera, Pseudococcidae) behavior of
pseudococci (Hymenoptera: Encyrtidae) in Sicilian males in response to sex-pheromone in laboratory and
vineyards. J Entomol Acarol Res 42(3):161170 eld. Ann Entomol Soc Am 77:3238
Martinez-Ferrer MT, Ripolles JL, Garcia-Mari F (2006) Mori K, Ueda H (1981) Pheromone synthesis. Part
Enumerative and binomial sampling plans for citrus XLV. Synthesis of the optically active forms of
mealybug (Homoptera: Pseudococcidae) in citrus 2,6-dimethyl-1,5-heptadien-3-ol acetate, the pheromone
groves. J Econ Entomol 99:9931001 of the Comstock mealybug. Tetrahedron 37:25812583
McCullough DW, Bhupathy M, Piccolino E, Cohen T Mudavanhu P, Addison P, Ken LP (2011) Monitoring and
(1991) Highly efcient terpenoid pheromone synthe- action threshold determination for the obscure mealy-
sis via regio and stereo controlled processing of bug Pseudococcus viburni (Signoret) (Hemiptera:
allylthiums generated by reductive lithiat. Tetrahedron Pseudococcidae) using pheromone-baited traps. Crop
47:97279736 Prot 30(7):919924
Mendel Z, Dunkelblum E, Branco M, Franco JC, Kurosawa Nakagawa N, Mori K (1984) Pheromone synthesis. Part
S, Mori K (2003) Synthesis and structure-activity rela- 69. New syntheses of (R)-(+)-3-acetoxy-2, 6-dimethyl-
tionship of diene modied analogs of Matsucoccus sex 1,5-heptadiene, the pheromone of the Comstock
pheromones. Naturwissenschaften 90:313317 mealybug. Agr Biol Chem Tokyo 48:27992803
Mendel Z, Protasov A, Zada A, Assael F, Jasrotia P, Franco Nakahata T, Itagaki N, Arai T, Sugie H, Kuwahara S
JC (2008) Longevity and sexual maturity of an adult (2003) Synthesis of the sex pheromone of the citrus
14 Semiochemicals in Mealybugs 197

mealybug, Pseudococcus cryptus. Biosci Biotechnol Identication of the California red scale sex phero-
Biochem 67:26272631 mone. J Chem Ecol 4:211224
Negishi T, Ishiwatari T, Asano S (1980a) Sex pheromone Rotundo G (1978) Mass isolation of virgin females of
of the Comstock mealybug, Pseudococcus comstocki Pseudococcus calceolariae (Mask.) (Homoptera,
Kuwana; bioassay method, male response-habits to Coccoidea) by the use of a juvenile hormone (Italian).
the sex pheromone [Japanese]. Jpn J Appl Entomol Bollettino del Laboratorio di Entomologia Agraria
Zool 24(1):15 Filippo Silvestri Portici 35:162168
Negishi T, Uchida M, Tamaki Y, Mori K, Isiwatari T, Asano Rotundo G, Tremblay E (1975) Sull attractivit delle
S, Nakagawa K (1980b) Sex pheromone of the comstock femmine vergini di due specie dePseudococcidi
mealybug, Pseudococcus comstocki Kuwana: isolation (Homoptera: Coccoidea) per un Imenottero parassita
and identication. Appl Entomol Zool 15:328333 (Hymenoptera Chalcidoidea). Boll Lab Entomol
Nestel D, Cohen H, Saphir N, Klein M, Mendel Z (1995) Agrar F Silvestri Portici 32:172179
Spatial distribution of scale insects comparative study Rotundo G, Tremblay E (1976) Simple extraction and bio-
using Taylors power-law. Environ Entomol 24:506512 assay of the female sex pheromone of the Citrus mealy-
Odinokov VN, Kukovinets OS, Isakova LA, Zainullin bug, Planococcus citri. Ann Appl Biol 82(1):165167
RA, Moiseenkov AM, Tolstikov GA (1984a) New Rotundo G, Tremblay E (1980) Evaluation of the daily rate
synthesis of the sex pheromone of Planococcus citri of sex pheromone release by the females of two mealy-
(Risso). Dokl Akad NaukSSSR+ 279:398401 bug species (Homoptera Coccoidea Pseudococcidae).
Odinokov VN, Kukovinets OS, Isakova LA, Zainullin Boll Lab Entomol Agrar F S Portici 37:167170
RA, Moiseenkov AM, Tolstikov GA (1984b) Rotundo G, Tremblay E (1982) Preliminary report on the
Ozonolysis of alkenes and study of reactions of poly- attractivity of the synthetic pheromone of Planococcus
functional compounds.43. Synthesis of (1R,3R)-(+)- citri (Rs.) (Homoptera:Coccoidea) in comparison to vir-
cis-1-acetoxymethyl-3-isopropenyl-2,2- gin females. Boll Lab Entomol Agrar F S 39:97101
dimethylcyclobutane sex pheromone of grape mealy Rotundo G, Gaston LK, Horey HH (1979a) Collection
bugs (Planococcus citri) and its (1S,3S)-()-cis- and purication of the female sex pheromone of
enantiomer. Zh Org Khim 27:555558 Pseudococcus calceolariae (Homoptera: Coccoidea).
Odinokov VN, Kukovinets OS, Isakova LA, Zainullin RA, Bollettino del Laboratorio di Entomologia Agraria
Moisunkov AM, Tolstikov GA (1991) Ozonolysis of Filippo Silvestri. Portici 36:160171
alkenes and study of reactions of polyfunctional com- Rotundo G, Tremblay E, Giacometti R (1979b) Final
pounds. 43. Synthesis of (1R 3R)-(+)-cis-acetoxy-methyl- results of mass captures of the citrophilous mealybug
3-isopropenyl-2,2-dimethyl cyclobutane- the sex males Pseudococcus calceolariae (Mask.) (Homoptera
pheromone of grape mealy bug (Planococcus citri) and its Coccoidea) in a citrus grove. Boll Lab Entomol Agrar
(1S, 3S)- ()-cis enantiomer. Zh Org Khim 27:555558 F S Portici 36:266274
Ortu S, Delrio G (1982) Osservazion sullimpiego in Rotundo G, Tremblay E, Papa P (1980) Short-range orien-
campo del feromone sessuali di sintesi di Planococcus tation of Pseudococcus calceolariae (Mask.) males
citri (Risso) (Homoptera: Coccoidae). Estratto da (Homoptera Coccoidea) in a wind tunnel. Boll Lab
Redia 65:341353 Entomol Agrar F S Portici 37:3137
Ortu S, Cocco A, Lentini A (2006) Utilisation of sexual Serebryakov EP, Suslova LM, Moiseenkov AM, Shavyrin
pheromones of Planococcus cus and Planococcus SV, Zaikina NV, Sorochinskaya AM, Kovalev BG
citri in vineyards. Bull OILB/SROP 29:207208 (1986) Terpenes in organic syntheses. 1. Synthesis of
Panis A (1981) Mealybugs (Homoptera, Coccoidea: (1R,3S)-1-(acetoxymethyl)-3-isopropenyl-2,2-
Pseudococcidae) within the framework of integrated dimethylcyclobutane (sex pheromone of the citrus
control in Mediterranean citrus-growing [French]. Rev mealybug) from verboxide. Ser Khim 7:16031607
Zool Agric Pathol Veg 78(3):8896 Serrano MS, Lapointe SL, Meyerdirk DE (2001)
Passaro LC, Webster FX (2004) Synthesis of the female Attraction of males by virgin females of the mealybug.
sex pheromone of the citrus mealybug, Planococcus Maconellicoccus hirsutus (Hemiptera:
citri. J Agric Food Chem 52:28962899 Pseudococcidae) Environ Entomol 30(2):339345
Powell W, Pickett JA (2003) Manipulation of parasitoids Shaw PW, Walis DR (2011) Pheromone trap and crop
for aphid pest management: progress and prospects. infestation monitoring of mealybug species in Nelson
Pest Manag Sci 59:149155 apple orchards. N Z Plant Protect 64:291
Rivera SB, Swedlund BD, King GJ, Bell RN, Hussey CE, Shaw P, Wallis D, Charles J (2012) Recent records of the
Shattuck-Eidens DM, Wrobel WM, Peiser GD, mealybug parasitoid Alamella mira Noyes
Poulter CD (2001) Chrysanthemyl diphosphate syn- (Hymenoptera: Aphelinidae) captured in citrophilus
thase: isolation of the gene and characterization of the mealybug (Pseudococcus calceolariae) sex phero-
recombinant non-head-to-tail monoterpene synthase mone traps in Nelson. The Weta 42:3437
from Chrysanthemum cinerariaefolium. Proc Natl Skatteboel L, Stenstroem Y (1989) Facile synthesis of
Acad Sci U S A 98:43734378 racemic 3-acetoxy-2,6-dimethyl-1,5-heptadiene, the
Roelofs WL, Gieselmann MJ, Carde AM, Tashiro H, sex pheromone of the Comstock mealybug. Acta
Moreno DS, Henrick CA, Anderson RJ (1978) Chem Scand 43:9396
198 N. Bakthavatsalam

Smetnik AI, Rozinskaya EM (1988) A new method is Pseudococcidae) in nurseries producing ornamental
introduced. Zashchita Rateni Moskva 3:4243 plants. J Econ Entomol 104(2):555565
Smith HS, Armitage HM (1920) Biological control of Wolk JL, Goldschmidt Z, Dunkelblum E (1986) A short
mealybugs attacking citrus. California Agric Expt Sta stereoselective synthesis of (+)-cisplanococcyl ace-
Bull 9:104158 tate, sex pheromone of the citrus mealybug
Sugie H, Teshiba M, Narai Y, Tsutsumi T, Sawamura N, Planococcus citri (Risso). Synthesis 4:347348
Tabata J, Hiradate S (2008) Identication of a sex Zada A, Dunkelblum E (2006) A convenient resolution of
pheromone component of the Japanese mealybug, racemic lavandulol through lipasecatalyzed acylation
Planococcus kraunhiae (Kuwana). Appl Entomol with succinic anhydride: simple preparation of enan-
Zool 43(3):369375 tiomerically pure (R)-lavandulol. Tetrahedron-
Tabata J, Narai Y, Sawamura N, Hiradate S, Sugie H Asymmetry 17:230233
(2012) A new class of mealybug pheromones: a hemi- Zada A, Harel M (2004) Enzymatic transesterication of
terpene ester in the sex pheromone of Crisicoccus racemic lavandulol: preparation of the two enantiomeric
matsumotoi. Naturwissenschaften 99(7):567574 alcohols and of the two enantiomers of lavandulyl sene-
Tashiro H, Chambers DL (1967) Reproduction in the cioate. Tetrahedron-Asymmetry 15:23392343
California red scale, Aonidiella aurantii (Homoptera: Zada A, Dunkelblum E, Assael F, Harel M, Cojocaru M,
Diaspididae). I Discovery and extraction of a female sex Mendel Z, Pellizzari G (2001) Identication of a sec-
pheromone. Ann Entomol Soc Am 60(6):935940 ond sex pheromone component of the vine mealybug.
Tauber O, Sternlicht M, Hefetz A (1985) Preliminary Boll Zool Agrar Bach 33(275):281
observations on the behavior of male Planococcus Zada A, Dunkelblum E, Assael F, Harel M, Cojocaru M,
citri exposed to the synthetic sex pheromone, with ref- Mendel Z (2003) Sex pheromone of the vine mealy-
erence to its applicability for population monitoring. bug, Planococcus cus in Israel: occurrence of a sec-
Phytoparasitica 13:148 ond component in a mass-reared population. J Chem
Teshiba M, Shimizu N, Sawamura N, Narai Y, Sugie H, Ecol 29:977988
Sasaki R, Tabata J, Tsutsumi T (2009) Use of a sex Zada A, Dunkelblum E, Harel M, Assael F, Gross S,
pheromone to disrupt the mating of Planococcus Mendel Z (2004) Sex pheromone of the citrus mealy-
kraunhiae (Kuwana) (Hemiptera: Pseudococcidae). bug Planococcus citri: synthesis and optimization of
Jpn J Appl Entomol Zool 53(4):173180 trap parameters. J Econ Entomol 97:361368
Thulasiram HV, Erickson HK, Poulter CD (2008) A com- Zada A, Dunkelblum E, Assael F, Franco JC, da Silva EB,
mon mechanism for branching, cyclopropanation, and Protasov A, Mendel Z (2008) Attraction of
cyclobutanation reactions in the isoprenoid biosyn- Planococcus cus males to racemic and chiral phero-
thetic pathway. J Am Chem Soc 130:19661971 mone baits: ight activity and bait longevity. J Appl
Uchida M, Nakagawa K, Negishi T, Asano S, Mori K Entomol 132(6):480489
(1981) Synthesis of 2,6-dimethyl-1,5-heptadien-3-ol Zhang AJ, Amalin D (2005) Sex pheromone of the female
acetate, the pheromone of the Comstock mealybug pink hibiscus mealybug, Maconellicoccus hirsutus
Pseudococcus comstocki Kuwana, and its analogs. (Green) (Homoptera: Pseudococcidae): biological
Agric Biol Chem Tokyo 45:369372 activity evaluation. Environ Entomol 34:264270
Ujita K, Saeki K (2008) Process for preparation of 2-isop Zhang AJ, Nie JY (2005) Enantioselective synthesis of the
ropenyl-5-methyl-4-hexen-1-yl 3-methyl-2-butenoate. female sex pheromone of the pink hibiscus mealybug,
PCT Int Appl Patent WO 2008075468 Maconellicoccus hirsutus. J Agric Food Chem
Unelius CR, El-Sayed AM, Twidle A, Bunn B, Zaviezo T, 53(7):24512455
Flores MF, Bell V, Bergmann J (2011) The absolute Zhang AJ, Amalin D, Shirali S, Serrano MS, Franqui RA,
conguration of the sex pheromone of the citrophilous Oliver JE, Klun JA, Aldrich JR, Meyerdirk DE,
mealybug, Pseudococcus calceolariae. J Chem Ecol Lapointe SL (2004) Sex pheromone of the pink hibis-
37(2):166172 cus mealybug, Maconellicoccus hirsutus, contains an
Vitullo J, Wang S, Zhang A, Mannion C, Bergh JC (2007) unusual cyclobutanoid monoterpene. Proc Natl Acad
Comparison of sex pheromone traps for monitoring Sci U S A 101:96019606
pink hibiscus mealybug (Hemiptera: Pseudococcidae). Zhang AJ, Wang SF, Vitullo J, Roda A, Mannion C, Bergh
J Econ Entomol 100:405410 JC (2006) Olfactory discrimination among sex phero-
Walton VM, Daane KM, Pringle KL (2004) Monitoring mone stereoisomers: chirality recognition by pink
Planococcus cus in South African vineyards with sex hibiscus mealybug males. Chem Sens 31:621626
pheromone-baited traps. Crop Prot 23:10891096 Zou YF, Millar JG (2011) Stereoselective synthesis of the
Walton VM, Daane KM, Bentley WJ, Millar JG, Larsen obscure mealybug pheromone by hydrogenation of a
TE, Malakar-Kuenen R (2006) Pheromone based mat- tetra substituted alkene precursor. Tetrahedron Lett
ing disruption of Planococcus cus (Hemiptera: 52(32):42244226
Pseudococcidae) in California vineyards. J Econ Zou YF, Daane KM, Bentley WJ, Millar JG (2010)
Entomol 99:12801290 Synthesis and bioassay of racemic and chiral trans-
Waterworth RA, Redak RA, Millar JG (2011) Pheromone- alpha-necrodyl isobutyrate, the sex pheromone of the
baited traps for assessment of seasonal activity and grape mealybug Pseudococcus maritimus. J Agric
population densities of mealybug species (Hemiptera: Food Chem 58(8):49774982
Ant Association
M. Mani and C. Shivaraju

The classic antaphid mutualistic relationship were also observed on grapevines in Europe in
has long been observed by naturalist and ento- association with Phenacoccus aceris (Signoret;
mologist alike, and several studies were con- Sforza 2008).
ducted on the actual/benets and factors involved
in these associations. This type of relationship
between ants and other insects is known to occur 15.1 Benets to Mealybugs
in a number of homopterous groups, especially in
the mealybugs. In the case of mealybugs, the Benets derived by mealybugs are more numer-
degree of dependence on the ants may vary from ous than might be expected.
strong and almost necessary associations to
weak, casual seasonal relationships. The associa-
tion of ants with the mealybugs resulted in the 15.2 Protection from Natural
hypothesis more the ants, more the mealybugs. Enemies
Ants are often associated with mealybugs as hon-
eydew consumers. Hemiptera-tending ants are Ants protect mealybugs from their natural ene-
mostly species of the subfamilies Myrmicinae, mies; this is a very important and long-realized
Dolichoderinae, and Formicinae (Degen and aspect of mealybug benet. Natural enemies are
Gersani 1989; Mittler and Douglas 2003). easily disturbed by movements of the ants. Ants
Samways et al. (1982) reported that 11 % of the are naturally hostile to any quick or obviously
123 ant species identied in citrus orchards in harmful movements around the honeydew
South Africa were associated with mealybugs. sources (Herzig 1938; Nixon 1951). The disrup-
Some mealybugs have an obligatory association tion of the activity of natural enemies by ants pro-
with ants: all Southeast Asian myrmecophilous vides a temporal refuge for mealybugs (Gutierrez
mealybugs have been collected only with ants of et al. 2008). Ants have long been known to aggra-
the genera Acropyga, Dolichoderus, or vate mealybug populations and other honeydew-
Polyrhachis, which attend the mealybugs either producing insect species by disrupting the natural
in subterranean nests or on aerial plant parts biological controls on these species.
(Gullan and Kosztarab 1997). Aboveground nests Ants deter the natural enemies of mealybugs.
There are numerous examples of ants deterring
M. Mani (*) C. Shivaraju the predators and parasites of mealybugs. For
Indian Institute of Horticultural Research, instance, ants also reduce parasitism of the cas-
Bangalore 560089, India sava mealybug, Phenacoccus manihoti

Springer India 2016 199

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_15
200 M. Mani and C. Shivaraju

Matile-Ferrero (Cudjoe et al. 1993). A wide vari- attending the sucking pests. In Kenya, C. mon-
ety of natural enemies are known to prey on pine- trouzieri, released for the control of Planococcus
apple mealybugs. Ants protect mealybugs from kenyae (LePelley), was eliminated by ants
their natural enemies (Gonzlez-Hernndez et al. (Anderson 1926). The ant Pheidole punctata
1999). In the eld, Pheidole megacephala (F. Smith) was known to destroy the larvae and
(Fabricius) had a positive association with adults of Cryptolaemus montrouzieri Mulsant
Dysmicoccus neobrevipes Beardsley and a nega- preying on Planococcus citri in South Africa
tive association with the predators of mealybugs (Kirkpatrick 1927). The ineffectiveness of C.
(Jahn and Beardsley 2000). Collectively, P. mega- montrouzieri against Planococcus citri (Risso) at
cephala deters predators from attacking D. neo- Liguria (Italy) was due to the attack of ants such
brevipes. Ants are known to attack the parasitoids as Tapinoma erratium nigerrimum Oryl and
and predators of scales and mealybugs while Iridomyrmex humilis Mayr (Constantino 1935).

Mealybugs and ants on a fruit Ants attending the mealybugs

of noni (Morinda citrifolia)

The presence of Argentine ant, I. humilis, Maconellicoccus hirsutus (Green) showed that
appeared to be partly responsible for the failure all C. montrouzieri introduced were killed and
of Cryptolaemus to become permanently estab- removed in 132.5 min. The mealybugs that asso-
lished in Bermuda (Bennett and Hughes 1959). ciated with ants are indeed protected from attack
In India, the failure of establishment of C. mon- by their predatory natural enemies, although
trouzieri in the mealybug-infested citrus orchards mealybugs and ants do not have an intimate asso-
of Assam was due to the activity of ant Oecophylla ciation (Lai YiChun and Chang NiannTai 2007).
smaragdina (Fab.) (Narayanan 1957). The con- There was an interaction involving the pink
trol of P. citri with Cryptolaemus was made inef- mealybug Sacchariococcus sacchari, the ant
fective in the presence of ant attendants (Panis Camponotus compressus (Fabricius), and the
and Brun 1971). Loss of results with C. mon- predator C. montrouzieri in sugarcane (Srikanth
trouzieri was caused by I. humilis in France et al. 2001). C. montrouzieri was found more in
(Greathead 1976). The ants Cremaster and numbers and proved successful against the
Iridomyrmex were known to prey on C. mon- mealybugs in the absence of ants (Van der Goot
trouzieri (Collins and Scott 1982). The failure of 1948; Murray 1982). In South Africa, the control
ant control is detrimental to biological control of of ants like I. humilis and Anoplolepis custodiens
citrus mealybug (Singh 1978; Narayanan 1957). F. aided the predator C. montrouzieri to give very
The observation of the protective behavior of P. good control of P. citri (Greathead 1971). Poutiers
megacephala against the attack of C. montrouz- (1922) also suggested protecting C. montrouzieri
ieri on the pink hibiscus mealybug from I. humilis in France.
15 Ant Association 201

Protection of mealybugs from predators

Associations among invasive species of ants However, some mealybug predators, such as
and mealybugs are very important in their suc- coccinellids, apparently become tolerated by ants
cess in new locations (Helms and Vinson 2002). by mimicking the waxy body cover of the mealy-
The Argentine ant Linepithema humile (formerly bugs (Daane et al. 2007). This condition of para-
Iridomyrmex humilis) (Mayr) is an example of an sitepredator adaptation is often observed. The
invasive ant species that is a signicant pest in type of ladybird beetle larva is usually very mealy
both natural and managed habitats, and it is com- in appearance and blends in well with its pseudo-
monly associated with mealybug outbreaks coccid host. Thus, the parasite or predator spe-
(Daane et al. 2006; Silverman and Brightwell cies is well adapted to the use of ant-attended
2008). hosts. Ladybird beetle predators are often found
Saying that ants protect mealybugs from among formicid attendants. Ants seem unable to
natural enemies does not necessarily mean that recognize the ladybird beetle larva as a predator.
ants are attacking the natural enemies to save There is, therefore, little doubt that the seemingly
honeydew as a food resource. Ants deter the nat- mimetic resemblance of the beetle larva to the
ural enemies of mealybugs (Jahn and Beardsley mealybug is an aid to its more perfect predaceous
1994; Rohrbach et al. 1988). The encyrtid para- habitat. Another possible mealybug parasite
sitoid Anagyrus ananatis Gahan of pineapple adaptation has been noted in a species of y
mealybug is not only scared away from when larva. This larva apparently remains outside its
ants are present but they are also rarely killed by hosts body and extracts food externally. This
predators such as the ladybird beetles. When ants habit would seem to make it readily susceptible
are absent, the parasitoid is highly effective in to the attack by ants. In order to overcome the
lowering the mealybug populations in pineapple problem, the larva is always found completely
plantings. Ant and mealybug interactions were hidden beneath the mealybug, and only when the
studied in a pineapple eld near Honolu on the host insect is removed can the larva be seen.
island of Maui, Hawaii. Big-headed ant Pheidole
megacephala was found to have a positive asso-
ciation with gray pineapple mealybug 15.3 Ant Constructions
Dysmicoccus neobrevipes but no association
with Dysmicoccus brevipes (Cockerell). Sticky Ants protect the mealybugs from adverse weather
trap collections revealed that D. neobrevipes and by building earthen shelters around them and
D. brevipes are dispersed by the wind. The posi- moving them to protected places; and some ant
tive association between P. megacephala and D. species actively construct shelters for mealybugs
neobrevipes was not due to ants transporting that provide some protection from unfavorable
mealybugs but could have resulted from ants environments and natural enemies (Franco et al.
deterring natural enemies or removing honeydew 2000; Helms and Vinson 2002; McLeod et al.
(Gary and Beardsley 2000). 2002). There are two main types of ant construc-
202 M. Mani and C. Shivaraju

tions which are important to mealybugs. The rst drops of rain, although the tent itself is in no way
is the actual ants nest and the second is the so- waterproof. Second, the tent, which has only one
called carton or ant tent. The latter is not important very small entrance, is important in shielding the
in California, although Wheeler (1926) mentioned mealybugs from large parasites. Apparently, the
several instances of carton nests in North mealybug parasites are unable to either nd the
America. Ant-nest isolation of the mealybugs is tent entrance or push their way through. Although
considered quite important and has been observed there are many records of tent parasitism, the rate
on several occasions in California. In one instance, of incidence is much lower than where no protec-
Phenacoccus artemisiae Ehrhorn was found in tion is afforded.
some of the upper chambers of a Crematogaster
nest. These mealybug specimens were found at
least 2 ft from the nearest host plant and in two 15.4 Removal of Honeydew
instances were being transported in the mandibles
of an ant. This particular collection was made in Ants prevent the accumulation of honeydew by
early February, which is a time of very low insect consuming it (Jahn and Beardsley 1994; Rohrbach
activity and high precipitation rate. The mealybugs et al. 1988). Honeydew accumulation, and the
were quiescent for the most part and were found in sooty mold that can grow on honeydew, may be
close contact with one another on the ceiling of ant detrimental to mealybugs. These ants, especially
nest chambers. It seems likely also that parasite P. megacephala, have been blamed for protecting
protection would be important. them against their natural enemies while remov-
Fungus is also a parasite of mealybugs, ing the excess honeydew produced by the mealy-
although infestation is not normally observed bugs (Gonzlez-Hernndez et al. 1999).
until the pseudococcid has been mounted; when One of the direct benets of ant association to
examining mealybug preparations, however, fun- mealybugs is shown in relation to the production
gus infestation is often seen. Ant-nest protection of honeydew and the subsequent contamination
from a highly humid environment is therefore an of the honeydew and source insect with sooty
important factor in mealybug welfare and is prob- mold. Because this fungus contaminant is often
ably directly connected with protection from fun- the cause of mass destruction of mealybugs, cer-
gus contamination. Protection from harsh winter tain adaptations have been made to rid the mealy-
conditions is perhaps the most important factor of bug of the secretion. Ants remove honeydew
ant-nest benet to mealybugs in California. from mealybugs, thereby preventing fungi from
For the most part, ant tents are important in the attacking mealybugs, and the removal of honey-
tropical areas, where two primary types are found. dew prevents contamination, which may be espe-
The rst is constructed with the silk-forming cially detrimental to rst-instar nymphs (Cudjoe
glands of the ant larvae. The adult, which has no et al. 1993; Daane et al. 2006, 2007; Gullan and
silk gland, holds a larva in its mandibles and forces Kosztarab 1997; Moreno et al. 1987). Rohrbach
the immature form to produce its silken product in et al. (1988) hypothesized that honeydew feeding
the desired area. The ant genus Oecophylla is well by ants could benet mealybugs by preventing
known for this habit. The second type of tent is the accumulation of honeydew on the mealybugs
made of earth, paper formed by the ant, and themselves. Presumably, immature mealybugs
leaves. Any or all of these materials may play a get stuck in honeydew and die if ants do not
role in the tent construction. The tents are nor- remove it. Phenacoccus alieni McKenzie is
mally built over mealybug colonies which may known to squirt a small globule of honeydew
have as many as 1,200 individuals. Tent dimen- from the anus to a distance of over 4 in.. This
sions have been recorded up to 4.5 2.3 in. distance is at least 20 times the total length of the
Mealybug-derived benets are twofold. First, insect and shows that mealybugs are quite capa-
the tent provides some protection from direct ble of ejecting honeydew to distances well out of
15 Ant Association 203

the range of their personal contamination. When nest. Ants are the primary or sole means of
ants are in attendance, they remove the honeydew mealybug dispersal in pineapple. Illingworth
as described above, thus eliminating the problem (1931) observed P. megacephala carrying mealy-
of sooty-mold contamination. Because of this, bugs from one cage of pineapples to another. The
ant-attended mealybug colonies are quite often big-headed ant Pheidole megacephala. (F.),
very dense with little distance between individu- Argentine ant Linepithema humile (Mayr), and
als to allow for honeydew ejection. re ant Solenopsis geminata (F.) are commonly
However, in Californias coastal vineyards, found in the Hawaiian pineapple agroecosystem,
Argentine ants increased densities of the obscure where they tend pink pineapple mealybugs
mealybug Pseudococcus viburni (Signoret), pri- (PPM) and gray pineapple mealybugs (GPM) for
marily by removing the honeydew that impedes honeydew. These ants, especially P. megaceph-
the movement of crawlers. Meanwhile, the larvae ala, have been blamed for dispersing mealybugs
of C. montrouzieri successfully forage in patches (Gonzlez-Hernndez et al. 1999).
of high mealybug density. One hypothesis is that
larvae of C. montrouzieri, being also covered
with waxy structures, successfully mimic mealy- 15.6 Benet to Ants
bugs and avoid detection by ants. Furthermore,
when approached by an ant, the coccinellid larva Access to honeydew has been shown to enhance
stops moving and lowers its body against sub- the rate of increase of ant colonies. Honeydew
strate, thus better resembling a sessile mealybug. accounts for more than half of the diet of many
The ants move around the larva, and stroke it temperate wood ants (Formica spp.), and it is the
with their antennae like they stroke the mealy- dominant food source of some subterranean ants
bug. After failing to obtain the honeydew, the ant (Mittler and Douglas 2003). Mealybug exudates/
moves away. Densities of C. montrouzieri were honeydew is highly acidic (pH 3) with fructose
higher on ant-tended vines, where there were (45 g), glucose (20 %), and other sugar contents
more mealybugs (Daane et al. 2007). in negligible quantity (02 %) per 100 g of solids
Ants stimulated increased feeding by mealy- (Ashbolt and Inkerman 1990). The normal ant
bugs; tending by the ants may have other effects mealybug association when observed in the eld
that alter mealybug densities: It may also improve is seemingly quite simple. The ants, which may
the mealybugs habitat or tness (Daane et al. be of various genera, normally move busily from
2007). In the presence of ants, mealybugs are one mealybug specimen to another. When a
able to ingest larger quantities of sap (Degen and mealybug is contacted, the ant begins to fondle
Gersani 1989). In several instances, ant-tended the mealybug with its antennae just as it might
mealybug colonies will be much larger than colo- fondle its own brood.
nies of the same mealybug species on the same The ants rest their heads on the dorsum of the
host that are not tended by ants. Therefore, out- mealybugs near the area of the ostioles for hon-
wardly the ants presence must be of some benet eydew. Mealybugs extrude a solution from their
to the mealybug, either directly or indirectly. ostioles when disturbed. This is possibly a
defense mechanism. When Phenacoccus echeve-
ria McKenzie is purposefully disturbed, it
15.5 Transportation of Mealybugs extrudes two small globules of honeydew through
its posterior ostioles. An ant then comes along
Ants are known to transport the mealybugs from and within a few seconds ingests all of the
plant to plant between and within elds, thus extruded honeydew. It is clear that ants benet
facilitating mealybug dispersal. In California, it from mealybugs in receiving honeydew from
is often possible to see ant Camponotus actually them, which is added to the ants food supply.
carrying from its host plant, directly into the ants The amount that ants rely on honeydew for their
204 M. Mani and C. Shivaraju

existence varies greatly with the species involved. 15.7 Predatory Effect of Ants
Some ants seem almost entirely unknown
whether this adaptation to aid in procuring hon- A nal direct benet not often realized, but per-
eydew, or whether this is the normally in an adap- haps a factor of importance in the understanding
tation to aid in procuring honeydew or whether of the biological control of mealybugs, is that
the normally indigestible wax is actually used in some ants actively regulate the population size of
ants diet. their hosts. It has been demonstrated that certain
ant species will actually keep the mealybug pop-
ulation down to a size which they can control,
thus eliminating production of honeydew. The
ants regulate any excessive build-up of popula-
tion by killing a number of mealybugs, and con-
suming the mealybugs is considered a supplement
to the protein portion of the ant diet (Way 1963).
This habit is also of importance in eliminating
sooty-mold contamination in the mealybug col-
ony. Some ant species may switch between tend-
ing and preying on mealybugs (Degen and
Gersani 1989; Mittler and Douglas 2003; Way
1963). The predatory role of ants on the mealy-
bugs is very meager in the regulation of
Globule of honeydew

A third and nal benet has been mentioned 15.8 Strange Aspects of Ant
earlier and deals with the use of associated Mealybug Associations
mealybug as a source of protein. Although preda-
ceous non-honeydew-consuming ants are not Exceedingly unusual observations were made by
known to attend mealybugs just for protein, some Bunzli in relation to an association between the
ants, which have both honeydew-consuming and mealybug Neorhizoecus coffeae (Laing) and the
predaceous habits, will occasionally kill mealy- ant Acropyga paramaribensis (Borgmeier). The
bugs and use them for protein. In nutritional eggs and immature mealybugs were kept in
value, honeydew is more complete than might be chambers with eggs and larvae of the ant. The
expected. It may contain free amino acids, immature female mealybugs apparently served as
amides, proteins, many minerals, and B vitamins honeydew sources. When the mealybug matured,
(Way 1963). The honeydew may vary greatly in it no longer produced honeydew and was then
its content depending on the species of mealy- transported by the worker ants to a separate
bug, the host plant, the age of plant, the part of mealybug chamber. The eggs that are laid by the
plant upon which mealybugs are feeding, and the mature females are then carried back to the brood
length of time that the insect feeds. Normally, a chambers. This association is not too unusual.
complete diet of honeydew will not compensate The extraordinary part of the relationship is the
for a protein deciency in the ant, and supple- fact that the winged virgin female ants, when
mentary protein must be added to correct the leaving the nest on their nuptial ight, always
situation. carry in their mandibles a fertilized female
There are several records of ants keeping mealybug. This mealybug will soon be the begin-
mealybugs pseudo wax-free. Ants might use ning of the honeydew source of a newly formed
mealybug wax for some nutritive value. Acropyga nest.
15 Ant Association 205

Another exceptional transport association is Hawaii. Ant and mealybug populations in

described by Reyne (1954) in Java. In this case, infested plots increased gradually and appeared
mealybug Hippeococcus is especially adapted to be strongly inuenced by the phenology of the
with long raptorial legs and sucker-like digitules pineapple plants during the rst fruit crop.
for clinging of Dolichoderus ants. When dis- Unusually heavy rainfall caused the dramatic
turbed, the highly mobile immature mealybugs reduction in ant populations observed then.
climb onto the bodies of the ants and are carried Highest ant population levels occurred about 3
into the nest where large colonies of mealybugs years after planting, when all untreated plots
are maintained. became nearly uniformly infested. The incidence
In California, an exceptional relationship of mealybug wilt was higher when the ants and
existed between the mealybug, Cryptoripersia mealybugs were more (John et al. 1982).
salina (Ehrhorn) and the ant Crematogaster. The
mealybugs are enclosed in a white-felted sac at
maturity under rocks. When a rock was over- 15.9 Management of Ants
turned, the mealybugs were all in one large cham-
ber in the ants nest and were in great numbers, The association of ants with the mealybugs by
mostly matured mealybugs. Once the rock had giving protection to natural enemies, transport of
been overturned, masses of ants poured from the mealybugs, and removal of honeydew from the
lower tunnels of the nest in pursuit of their hon- mealybug colonies has resulted in an increase in
eydew symbionts. Within a matter of 15 min the mealybug population. It serves the basis to
the mealybug chamber had been emptied of its develop the hypothesis more the ants, more the
mealybug contents. mealybugs. Hence, it is necessary to check the
Another unusual observation was made in activity of ants in the suppression of mealybugs.
Modoc County involving an association between According to Mansou et al. (2012), the ants
the mealybug Phenococcus colemani Ehrhorn Tapinoma nigerrimum constitute a threat to bio-
and the ant Formica subpolita. This mealybug is logical control of Planococcus cus (Signoret)
very often found in cracks and pits on the under- and Pl. citri in the orchards in Italy by either the
side of larvae rocks. When the mealybug-infested encyrtid parasitoids Anagyrus pseudococci
rock was distributed, associated ants hurriedly (Girault) and Leptomastix dactylopii (How.) or
tore the mealybugs, waxy sacs and all, from their larval stage of the coccinellid predator
rock habitat and carried them into cracks in the Cryptolaemus montrouzieri, and hence an ade-
soil. The ants removed the mealybug so rapidly quate control of the ants is highly recommended
that, in order to collect sufcient numbers of the before the release of any of these natural
mealybugs, the ants had to be removed rst. enemies.
Another unusual observation was made in General ant control measures may be adopted
Nevada. Ants were busily tending their mealybug to suppress the activity of ants. It has been sug-
host in the usual fondling manner. In this case, gested to apply a band of diazinon granules
the mealybugs were withholding their honeydew around the plant about 1 ft from the main stem.
supply from the ants. The ants, however, had Other control measures include destruction of ant
overcome this problem by butting the abdomen holes, red ant nests, and skirting of trees after
of the mealybug with their heads, thus causing fruit harvest, which prevents the ant migration
the honeydew to ow from the mealybug osti- through side branches. After the patrolling (up
oles. The ants then consumed the solution. and down) of ants on the trunk is stopped, the
There was another kind of interrelationships beetles can be released (Singh 1978). It was also
of big-headed ants, mealybugs, and spread of suggested that ants should be prevented by rub-
mealybug wilt disease. The big-headed ant, bing magnesia or powdered tale in a 4-in.-wide
Pheidole megacephala (Fabricius), is the domi- band at the time of liberation of Cryptolaemus
nant ant species in most of the pineapple elds in (Constantino 1935). Mealybug-infested custard
206 M. Mani and C. Shivaraju

apple plants were applied with sticky bands an acceptable level in 23 years. The baits need
which had helped to prevent the movement of to be placed in the eld during budbreak (March
ants (Murray 1982). BHC solution (5 g/l) was to June, depending upon location in the state) at a
poured into the anthills prior to the release of C. rate of 1520 bait stations (UC bait station) per
montrouzieri against Ferrisia virgata (Cockerell) acre (Nyamukondiwa and Addison 2011). Ants
in guava orchards (Mani et al. 1990). In the can also be managed by applying tanglefoot
orchards where ants were partially excluded, a every 12 weeks.
signicant reduction in citrus mealybug popula-
tions and damage could be observed (Villalba
et al. 2006). Applying a 6 % solution of chlorpy- References
riphos to the base of the vine and supporting
stake and to the surrounding soil gave the best Anderson TJ (1926) Report of entomologist. Rep Dept
Agric Kenya 135147
Ashbolt NJ, Inkerman PA (1990) Acetic acid bacterial
Liquid ant baits were evaluated for the control biodata of the pink sugar cane mealybug
of Argentine ants Linepithema humile (Mayr) Sacchariococcus sacchari and its environs. Appl
and associated mealybug pests (Pseudococcus Environ Microbiol 56(3):707712
Beardsley JW, Su TH, McEwen FL, Gerling D (1982)
species) in commercial vineyards. In all trials,
Field investigations of the interrelationships of the
liquid baits were an insecticide dissolved in 25 % big-headed ant, the gray pineapple mealybug, and
sugar water. In 2002, a liquid bait thiameth- pineapple mealybug wilt disease in Hawaii. Proc
oxam, mixed at 0.0001 % (active ingredient, Hawaii Entomol Soc 24:5167
Bennett FD, Hughes IW (1959) Biolgoical control of
A.I.) was delivered in ground-based (site 1) and
insect pests of Bermuda. Bull Entomol Res
canopy-based (site 2 and 3) dispensers that were 50:423436
recharged every 2 weeks and cleaned every 4 Chun LY, Tai CN (2007) The association of pink hibiscus
weeks, and deployed at rates of 160 (sites 1 and mealybug, Maconellicoccus hirsutus (Green) with
bigheaded ant Pheidole megacephala (Fabricius) on
2) and 620 (site 3) dispensers per hectare. There
hibiscus [Chinese]. Formosan Entomol 27:229243
was a signicant reduction of season-long ant Collins L, Scott JN (1982) Interactions of ants, predators
densities in liquid bait treatments at all sites and and the scale insect Pulvinariella mesembryanthem on
of mealybug densities at two of three sites; crop Carpobrotus edulis, an exotic plant naturalized in
Western Australia. Aust Entomol Mag 8(5):7375
damage was signicantly lower in the liquid bait
Constantino G (1935) Unnemicodel contonela degli-
treatment at all sites. Similarly, studies in the agrumi: Cryptolaemus montrouzieri Muls. Acireale R
pineapple eld showed that eradication of the Staz Sper de Fruttic e Agrumic Bol (ns) 6:7
ants reduced the population of mealybug Cudjoe AR, Neuenschwander P, Copeland MJW (1993)
Interference by ants in biological control of the cas-
(Beardsley et al. 1982).
sava mealybug Phenacoccus manihoti (Hemiptera:
Gourmet ant bait (Innovative Pest Control Pseudococcidae) in Ghana. Bull Entomol Res
Products, Florida USA), containing 1 % diso- 83:1522
dium octaborate tetrahydrate toxicant, dissolved Daane KM, Sime KR, Hogg BN, Bianchi ML, Cooper
ML, Rust MK, Klotz JH (2006) Effects of liquid
in 25 % sucrose solution to make 0.5 % A.I., was
insecticide baits on Argentine ants in Californias
overall the most preferred bait for Argentine ants coastal vineyards. Crop Prot 25:592603
Linepithema humile (Mayr), common pugna- Daane KM, Sime KR, Fallon J, Cooper ML (2007)
cious ants Anoplolepis custodiens (F. Smith) and Impacts of Argentine ants on mealybugs and their
natural enemies in Californias coastal vineyards. Ecol
cocktail ants Crematogaster peringueyi (Emery)
Entomol 32:583596
during spring, summer, and autumn, and on some Degen AA, Gersani M (1989) Environmental effects on
occasions being signicantly more preferable to activity and honeydew collection by the weaver ant
ants than the control solution. Management of Polyrhachis simplex (Hymenoptera, Formicidae)
when attending the mealybug Trabutina sp
Argentine ants is important in mealybug manage-
(Homoptera, Pseudococcidae). J Zool 218:421432
ment in a vineyard because the ants will protect Franco JC, Silva EB, Carvalho JP (2000) Mealybugs
the mealybugs. Ant baits, placed in approved dis- (Hemiptera, Pseudococcidae) associated with citrus in
pensers, can reduce Argentine ant populations to Portugal. ISA Press, Lisbon (in Portuguese)
15 Ant Association 207

Gary CJ, Beardsley JW (2000) Interactions of Ants McLeod P, Diaz J, Vasquez L, Johnson DT (2002) Within-
(Hymenoptera: Formicidae) and Mealybugs plant distribution and sampling of mealybugs in plan-
(Homoptera: Pseudococcidae) on Pineapple. Proc tain var. FHIA 21. Trop Agric 79:150153
Hawaii Entomol Soc 34:161165 Mittler TE, Douglas AE (2003) Honeydew. In: Resh VH,
Gonzlez-Hernndez H, Johnson MW, Reimer NJ (1999) Card RT (eds) Encyclopedia of insects. Academic,
Impact of Pheidole megacephala (F.) (Hymenoptera: Amsterdam
Formicidae) on the biological control of Dysmicoccus Moreno DS, Haney PB, Luck RF (1987) Chlorpyrifos and
neobrevipes (Cockerell) (Homoptera: diazinon as barriers to argentine ant (Hymenoptera,
Pseudococcidae). Biol Control 15(2):145152 Formicidae) foraging on citrus trees. J Econ Entomol
Greathead DJ (1971) A review of biological control in the 80:208214
Ethiopian region. Common Inst Biol Control Tech Murray DAH (1982) Effects of sticky banding of custard
Comm 5:162 apple tree trunks on ants and citrus mealybug
Greathead DJ (1976) A review of biological control in Planococcus citri (Risso) (Pseudococcidae,
western and Southern Europe. Common Inst Biol Hemiptera) in South Eastern Queensland. Queensland
Control Tech Comm 7:182 J Agric Animal Sci 39:141146
Gullan PJ, Kosztarab M (1997) Adaptations in scale Narayanan R (1957) A note on the performance of
insects. Annu Rev Entomol 42:2350 Cryatolaemus montrouzieri Bul. in citrus orchards at
Gutierrez AP, Daane KM, Ponti L, Walton VM, Ellis CK Burnihat (Assam). Tech Bull Commonw Inst Biol
(2008) Prospective evaluation of the biological control Cont 9:137138
of vine mealybug: refuge effects and climate. J Appl Nixon GEJ (1951) The association of ants with aphids and
Ecol 45:524536 coccids. Commonwealth Institute of Entomology,
Helms KR, Vinson SB (2002) Widespread association of London, 36 p
the invasive ant Solenopsis invicta with an invasive Nyamukondiwa C, Addison P (2011) Preference of forag-
mealybug. Ecology 83:24252438 ing ants (Hymenoptera: Formicidae) for bait toxicants
Herzig J (1938) Ameisen und Blattlause. Ztschr f Angew in South African vineyards. Crop Prot 30:10341038
Ent 24:367435 Panis A, Brun J (1971) Biological control tests against
Illingworth JF (1931) Preliminary report on evidence that three species of psuedococcidae (Homoptera:
mealybugs are an important factor in pineapple wilt. Coccoidea) in green house. Revue Zool Agric Path
J Econ Entomol 24:877889 Veg 70:4247
Jahn GC, Beardsley JW (1994) Big-headed ants, Pheidole Poutiers R (1922) Lacclimitation de Cryotolaemus mon-
megacephala: interference with the biological control trouzieri Muls. Dans le midi de la France Ann des
of gray pineapple mealybugs. In: Williams DF (ed) Epiphyt 8:318
Exotic ants: biology, impact and control of introduced Reyne A (1954) Hippeacoccus, a new genus of
species. Westview Press, Oxford, pp 199205 Pseudococcidae from Java with peculiar habits.
Jahn GC, Beardsley JW (2000) Interactions of ants Leyden Rijks Mues Van Natuurlijke His Zool Meded
(Hymenoptera: Formicidae) and mealybugs 32:233257
(Homoptera: Pseudococcidae) on pineapple. Proc Rohrbach KG, Apt WJ (1986) Nematode and disease
Hawaii Entomol Soc 34:181185 problems of pineapple. Plant Dis 70:8187
John W, Jr B, Sip TH, McEwen FL, Gerling D (1982) Rohrbach KG, Beardsley JW, German TL, Reimer NJ,
Field investigations on the interrelationships of the Sanford WG (1988) Mealybug wilt, mealybugs, and
big-headed ant, the gray pineapple mealybug, and ants of pineapple. Plant Dis 72(7):558565
pineapple mealybug wilt disease in Hawaii! Proc Samways MJ, Nel M, Prins AJ (1982) Ants (Hymenoptera:
Hawaiian Entomol Soc 24(1):5167 Formicidae) foraging in citrus trees and attending
Kirkpatrick ZW (1927) Biological control of insect pests honey-producing Homoptera. Phytophylactica
with particular reference to the control of common 14:155157
mealybug in Kenya colony. In: Proceedings of the Sforza R (2008) Les cochenilles sur la vigne. In: Bordeaux
South and East Africa Agricultural Conference 1926, Feret (ed) Les ravageurs de la vigne, pp 188210, 389
pp 184196 p
Mani M, Krishnamoorthy A, Singh SP (1990) The impact Silverman J, Brightwell RJ (2008) The Argentine ant:
of the predator, Cryptolaemus montrouzieri Mulsant, challenges in managing an invasive unicolonial pest.
on pesticide-resistant populations of the striped mealy- Annu Rev Entomol 53:231252
bug, (Ckll.) on guava in India. Insect Sci Appl Singh SP (1978) Propagation of a coccinellid beetle for
11(2):167170 the biological control of citrus and coffee mealybugs.
Mansou R, Suma P, Mazzo G, Pergola AS, Pappalardo V, Scientic Conference, CPA, 2 p
Lebdi KG, Russo A (2012) Interactions between the Srikanth J, Easwaramoorthy S, Kurup NK (2001)
ant Tapinoma nigerrimum (Hymenoptera: Formicidae) Camponotus compressus F. interferes with
and the main natural enemies of vine and citrus mealy- Cryptolaemus montrouzieri Mulsant activity in sugar-
bugs (Hemipotera: Pseudococcidae). Biocontrol Sci cane. Insect Environ 7:5152
Technol 22(5):527537
208 M. Mani and C. Shivaraju

Van der Goot P (1948) Biologishe bestrijding van vitte Pseudococcidae), in citrus orchards [Spanish]. Boletin
luis (Phenacoccus iceryoides) on kofe n de foradja- de Sanidad Vegetal Plagas 32(2):203213
landen (Ziuid Colebes). Meded Alg Proefstn Landb Way MJ (1963) Mutualism between ants and honeydew-
64:12 producing Homoptera. Annu Rev Entomol 8:307344
Villalba M, Vila N, Marzal C, Garcia Mari F (2006) Wheeler WM (1926) Ants, their structure, development
Inuence of inoculative releases of natural enemies and behaviour. Columbia University Press, New York,
and exclusion of ants in the biological control of the 663 p
citrus mealybug Planococcus citri (Hemiptera:
Methods of Control
M. Mani and C. Shivaraju

Mealybugs pose a serious threat to several agri- ior of mealybugs may provide a spatial refuge
cultural and horticultural crops throughout the from natural enemies and harsh environmental
world. They are a major problem in greenhouses conditions (Berlinger and Golberg 1978;
and nurseries, where they often cause severe eco- Gutierrez et al. 2008a). This type of plant coloni-
nomic damage. It seems surprising that such a zation makes mealybugs practically invisible
delicate soft-bodied insect is so difcult to con- during the latent population phase. However, dur-
trol. There are, however, several reasons which ing outbreaks, the population boils over from
may account for this fact. the refuge and becomes conspicuous. In addition,
Mealybugs developed several different other species have the habit of spending their
defense mechanisms. Many of the species tend to entire lives deep in the soil, protected almost
establish themselves in protected sites, such as from insecticidal materials.
cracks and crevices in bark, leaf axils, root Mealybugs are noted for the production of
crowns, nodes of grass stems, under fruit sepals dermal wax secretions. Adult mealybugs and the
and within fruit navels, between touching fruits nymphal instars are covered with waxy coating.
or fruits and leafs, and in tunnels bored by insect Also the eggs of mealybugs, protected by the
larvae in roots and stems (Franco et al. 2000; waxy lamentous secretions of the ovisac, are
Kosztarab and Kozr 1988). This cryptic behav- almost impossible to reach with insecticides.

M. Mani (*) C. Shivaraju

Indian Institute of Horticultural Research,
Bangalore 560089, India

Springer India 2016 209

M. Mani, C. Shivaraju (eds.), Mealybugs and their Management in Agricultural
and Horticultural crops, DOI 10.1007/978-81-322-2677-2_16
210 M. Mani and C. Shivaraju

Eggs protected with waxy ovisac Adult mealybug covered with Mealybug crawlers not covered