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Integrated Pest Management Reviews 5: 241–254, 2000.
© 2001 Kluwer Academic Publishers. Printed in the Netherlands.
Biological control of the hibiscus mealybug, Maconellicoccus hirsutus Green
(Hemiptera: Pseudococcidae) in the Caribbean
Moses T.K. Kairo, Gene V. Pollard1 , Dorothy D. Peterkin & Vyjayanthi F. Lopez
CABI Bioscience, Caribbean and Latin American Center, Gordon Street, Curepe, Trinidad and Tobago
1Food and Agriculture Organization of the United Nations, Sub-Regional Office for the Caribbean,
P.O. Box 631-C, Bridgetown, Barbados
∗Author for correspondence (Tel.: (+1) 868 645 7628; Fax: (+1) 868 663 2859; E-mail: m.kairo@cabi.org)
Accepted in final form 16 July 2001
Key words: biological control, Maconellicoccus hirsutus, Pseudococcidae, mealybug, Anagyrus kamali,
Cryptolaemus montrouzieri
Abstract
The hibiscus mealybug, Maconellicoccus hirsutus Green, was first reported in the Caribbean in 1994 in Grenada.
This was the first record of the insect as a major pest in the New World. By the beginning of 2001, the pest had spread
to over 25 territories from Guyana and Venezuela in the South to Bahamas in the North. The pest has also extended
its distribution to Central America (Belize) and North America (California, USA). Early attempts to control the pest
using pesticides resulted in failure and a classical biological control approach was adopted. Several exotic natural
enemies were introduced but control was attributed to Anagyrus kamali Moursi and Cryptolaemus montrouzieri
Mulsant. In all countries where biological control was implemented, this resulted in success. This paper reviews
the remarkable success story. Information is provided on the distribution and factors leading to rapid spread of the
pest, its pest status and resultant economic losses, and implementation of the biological control effort.
Introduction
The hibiscus mealybug (HMB), Maconellicoccus
hirsutus Green (Hemiptera: Pseudococcidae) was accidentally
introduced into the Caribbean in the early
1990s. It was first reported in Grenada in 1994
after which it rapidly spread through countries in the
Caribbean, becoming one of the most important pest
species. Initial measures to control the pest using chemical
and cultural measures were costly, difficult to
implement and/or ineffective (Pollard 1997; Sagarra &
Peterkin 1999). As an exotic pest, HMB was a good target
for classical biological control and efforts to achieve
this were initiated in 1995 in Grenada through a Technical
Cooperation Project of the Food and Agriculture
Organization (FAO) of the United Nations and executed
by CABI Bioscience. This led to the introduction
of the endo-parasitoid Anagyrus kamali Moursi
(Hymenoptera: Encyrtidae). Subsequently, and as the
pest spread to other countries, other agencies became
involved and more natural enemies were introduced,
most notably Cryptolaemus montrouzieri Mulsant
(Coleoptera: Coccinellidae). What happened next was
the dream of any biological control practitioner. Within
a short space of time pest populations were brought
under control and the results were replicated in each
country which became infested. With few exceptions
much of the information arising from this programme
has only been reported in local or regional publications.
This paper gives an account of the pest with particular
emphasis on the biological control effort.
Origin, distribution and spread
HMB is native to parts of Asia (Williams 1996). Prior to
its appearance in the Caribbean, the pest was known to
have a wide distribution in parts of Asia and Africa (IIE
1997). However, it had only ever been reported as a serious
pest in Egypt and India. The only previous record of

242 M.T.K. Kairo et al.
the pest in the New World is from Hawaii in 1983. However,
in stark contrast to the situation in the Caribbean, it
never became serious presumably because natural enemies
were fortuitously introduced with it (Beardsley
1985). Between 1994 and the present, the pest has
spread to over 25 territories in the Caribbean Basin,
from Guyana and Venezuela in the south to Bahamas in
the north and Belize and California in the west. Table 1
gives the distribution of M. hirsutus in the region up to
June 2001.
The pest appears to be inadvertently spread by
human beings. The rapid spread within the region was
remarkable, considering that many of the territories are
islands. It is envisaged that an understanding of the key
factors that may have led to this rapid spread would be
Table 1. Distribution of M. hirsutus in the Caribbean
and adjacent regions
Country Date of reporting
Grenada and Carriacou November 1994
Trinidad and Tobago August 1995/
November 1996
St. Kitts and Nevis
Netherlands Antilles
November 1995/
December 1995
Aruba ?
Sint Maarten September 1996
St. Eustatius May 1997
Curaçao June 1997
Saint Lucia October 1996
Anguilla 1996?/February 1997
Guyana April 1997
British Virgin Islands
(Tortola)
May 1997
St. Vincent and
the Grenadines
United States Virgin Islands
May 1997
St. Thomas May 1997
St. John May 1997
St. Croix June 1997
Montserrat January 1998
Guadeloupe
Puerto Rico
April 1998
Culebra December 1997
Vieques June 1997
PR Mainland April 1998
USA: California
(Imperial County)
August 1999
Belize (Belize City,
Belmopan)
September 1999
Venezuela
(Margarita Island)
November 1999
Barbados August 2000
Bahamas December 2000
Antigua February 2001
Dominica June 2001
useful in planning for similar situations in future. These
factors are listed below:
(a) frequent movement of people and goods fostered
by close intra-regional economic and cultural linkages,
(b) as with other plant sucking mealybugs and scales,
intimate association with its host plants increased
chances of spread through movement of plant
material,
(c) wide host range including many agricultural crops
as well as ornamentals which were frequently
moved between the territories,
(d) first instar nymphs and ovisacs could be easily
moved on passenger clothing,
(e) short distances between territories, thus chances
that insects may easily survive the journey were
high,
(f) quarantine was difficult for a pest with such a wide
host range and furthermore, quarantine services
were (and continue to be) under-resourced in many
of the countries,
(g) existence of a thriving informal trade between
some of the islands which was difficult to police
from a quarantine perspective,
(h) the public seemingly unaware of the risks posed by
the pest and was thus likely to move plant material
between different territories,
(i) the fact that the pest may have remained unidentified
for some time in Grenada led to build up of
very high populations which increased the chances
of accidental movement.
Feeding and damage symptoms
HMB attacks new flush growth, young shoots, flowers
and fruits. Both nymphs and female adults cause direct
damage by sucking plant sap from the phloem. While
feeding, HMB injects the plant with its toxic saliva,
which causes growth malformation characterized by
curling and crinkling of leaves. These are usually some
of the first noticeable symptoms of HMB presence.
Continued feeding causes stunting, with shortening
of internodes, deformed leaves and thickened twigs.
Heavy infestations may result in plant death. Infested
flowers often drop and usually there is little or no fruit
production. Infested fruits are small and deformed,
resulting in reduced production and marketability. The
insects also produce large quantities of honeydew
which encourages growth of black sooty molds on the
leaves. This results in reduced photosynthetic capacity.

Biological control of Maconellicoccus hirsutus 243
HMB also produce white fluffy wax which covers most
stages as well as the ovisac. The wax is protective in
function and is impermeable to water and most pesticides.
The presence of large quantities of wax reduces
the aesthetic and commercial value of ornamentals.
Pest status and host range
In Egypt, Albizia lebbek (Leguminosae), mulberry
(Morus alba: Moraceae) and Hibiscus spp.
(Malvaceae) were most severely affected (Bartlett
1978). In India, HMB was initially a serious pest of
fibre crops such as jute (Corchorus spp.: Tiliaceae),
mesta (Hibiscus cannabinus) and roselle (Hibiscus
sabdariffa). Later, it became a major pest of grapevines
(Vitis vinifera: Vitaceae) requiring regular intervention.
Globally, HMB has been reported on more than 200
plant species (Stibick 1997). At the height of HMB
outbreaks in the Caribbean, over 170 plant species
were attacked in Grenada, Trinidad and Tobago and
St. Kitts. These included fruit and forest trees, ornamental
shrubs, annual crops and weeds (McComie
1997). The list of affected species included all plants
on which the mealybug was found and/or showed
damage symptoms. Kairo (1997) suggested that when
large numbers of crawlers produced on suitable hosts
such as samaan (Samamea saman) were dispersed by
wind, these settled indiscriminately on a wide range of
plants. Many of these were incidental hosts on which
crawlers were able to establish and produce symptoms,
but which were not suitable for supporting mealybug
development and reproduction. Such plants were still
recorded as hosts although it has now been shown that
HMB is not economically important in many vegetable
crops reported as host plants. Indeed, once pest populations
were brought under control by the introduction
of natural enemies, fewer than 20 plant species were
found to support significant infestations of the HMB
(Table 2).
Economic losses
HMB is perhaps one of the few Caribbean pests for
which a detailed analysis of economic loss has been
undertaken, at least in some of the affected countries.
Different approaches were used in different countries
to estimate the losses but generally they have included
an assessment of direct loss to production and in some
cases losses due to trade restriction and cost of control.
In Grenada, Francois (1996) estimated one-time
Table 2. An indicative list of important host plants of M. hirsutus
in the Caribbean (Kairo 1997)
Type of plant Common name Scientific name
Ornamental Ornamental hibiscus Hibiscus rosa-sinensis
Ginger lily Alpinia purpurea
Forest trees Blue mahoe Hibiscus elatus
Samaan Samanea saman
Teak Tectona grandis
Hog plum Spondias mombin
Fruit trees/ Soursop Annona muricata
other crops Sugar apple Annona squamosa
Red plum Spondias purpurea
Yellow plum S. purpurea var lutea
Carambola Averrhoa carambola
Barbados cherry Malpighia glabra
Sapodilla Manilkara zapota
Ochro Abelmoschus
esculentum
Sorrel Hibiscus sabdariffa
Cotton Gossypium hirsutum
Cocoa Theobroma cacao
Citrus Citrus spp.
Weeds Man-better-man Achryanthes indica
Broomweed Sida spp.
losses at EC$ 9.7 million (US$ 3.6 million) and annual
losses at EC$ 9.3 million (US$ 3.5 million) but with
the recognition that losses to the Grenadian economy in
general were expected to be substantially higher. However,
these estimates did not include costs associated
with loss of trade or control of the pest. More recent
data which include these elements estimate losses in
Grenada for the period 1995–1998 at US$ 18.3 million
(Peters 1999). The costs of the control programme for
the period were estimated at EC$ 2.9 million (US$ 1.1
million). In St. Kitts, Francis (1999) estimated that for
the period October 1995 to January 1997, economic
losses amounted to US$ 280,000 inclusive of control
costs. Additionally, in 1997 onion production experienced
a loss of over US$ 22,000 in exports to regional
markets. Potential losses to agriculture and forestry
in Trinidad and Tobago were estimated at US$ 125
million (PMC 1996). However, in a recent study of
the socio-economic impact of the hibiscus mealybug
in Trinidad (Singh 1999) it was indicated that costs
of over US$ 5.1 million were incurred up to 1997.
At the same time, estimated net benefit for the period
1996–2024 was US$ 41 million. This represented a
socio-economic benefit/cost ratio of 8 : 1. Other reports
of the economic impact of this pest indicated some US$
67,000 for St. Lucia (Anon. 1999a) and US$ 3.4 million
for St. Vincent and the Grenadines (Edwards 1999).
Guyana, on the other hand, suffered no direct crop

244 M.T.K. Kairo et al.
production losses up to March 1999, as the pest never
invaded production areas. However, there was an uncalculated
economic impact on the agricultural sector due
to loss of regional export markets (Anon. 1999b). In a
recent analysis, the potential losses in the USA were
estimated at US$ 750 million per year (Moffit 1999).
Agricultural crops in the mainland US expected to bear
most of the economic risk were ornamentals, vegetables,
citrus, cotton, grapes and avocados. This interesting
analysis is based on the projected distribution of
HMB predicted by CLIMEX modeling.
Biological control
Biological control initiatives
The biological control effort was initiated in 1995
when the FAO funded a project for Grenada (TCP/
GRN/4553). Through the project, CABI Bioscience
assisted with the introduction of A. kamali, an
encyrtid parasitoid of the mealybug from China.
When Trinidad became infested in 1996, CABI
Bioscience also assisted with introduction of the
parasitoid in a project funded by the Trinidad
and Tobago Government. At the same time, the
Caribbean Agricultural Research and Development
Institute (CARDI) assisted with introduction of two
coccinellids, C. montrouzieri and Scymnus coccivora
Ramakrishna Ayyar (Coleoptera: Coccinellidae), from
India. Faced with a rapidly spreading problem, governments
in the region requested assistance from FAO
to deal with the situation. In 1996, a regional project
was approved. Initially, the beneficiary countries of the
project included all 13 independent Caribbean Community
(CARICOM) member countries (Antigua and
Barbuda, Bahamas, Barbados, Belize, Commonwealth
of Dominica, Grenada, Guyana, Jamaica, St. Kitts and
Nevis, Saint Lucia, St. Vincent and the Grenadines,
Suriname, Trinidad and Tobago) and Venezuela. Subsequently,
Cuba was also included as a beneficiary
country. The overall objective of the project was to
support regional activities towards a long-term sustainable
control of the HMB in the Caribbean Sub-
Region. There were three broad areas of activity under
the project – the actual biological control programme, a
public awareness component and training. CABI Bioscience
was responsible for the biological control component,
while CARDI was responsible for the public
awareness. The training component was undertaken as
a joint activity. An important component of the project
involved advisory missions to countries. These missions
were carried out jointly by scientists from CABI
Bioscience, FAO and CARDI.
In 1996, the United States Department of Agriculture,
Animal and Plant Health Inspection Service
(USDA-APHIS) in collaboration with the Ministry
of Agriculture St. Kitts and Nevis, initiated a parallel
program. CABI Bioscience provided an initial
stock of A. kamali which was multiplied and released,
while stocks of C. montrouzieri were obtained from a
commercial insectary in the USA. Indeed, most other
countries that implemented biological control subsequently
obtained stocks of C. montrouzieri from the
same source. In addition USDA-APHIS initiated an
exploratory programme through which another parasitoid,
Gyranusoidea indica Shafee, Alam and Agarwal
(Hymenoptera: Encyrtidae) collected in Egypt, was
introduced. USDA-APHIS activities were subsequently
transferred to St. Thomas, US Virgin Islands
and Puerto Rico, where these were focussed on control
of the pest in US Territories in the Caribbean. USDA-
APHIS was also instrumental in the organization of
several technology transfer workshops and the production
of a training manual (Meyerdirk et al. 1998).
CARINET, the Caribbean LOOP of BioNet International
in collaboration with CABI Bioscience and other
agencies was instrumental in organizing two regional
training workshops in mealybug identification. This
resulted in the production of an identification manual
in English and Spanish (Watson & Chandler 1999,
2000). The Inter-American Institute for Cooperation in
Agriculture (IICA) also assisted capacity building and
in collaboration with CARDI addressed post harvest
issues (Gautam et al. 2000; IICA 1999).
A vital component of the biological control efforts
was the part played by national institutions. Most of
the countries established national taskforces to specifically
deal with the problem. In affected countries, these
taskforces dealt with the tactical issues with regard to
control. In threatened countries, they played a more
strategic role both in planning detection programs and
eventual control. In some cases they were also responsible
for dealing with matters relating to trade.
Natural enemies of HMB and use in
biological control
The natural enemy complex of HMB in India and Egypt
is well known (Kamal 1951; Ghose 1970; Beardsley
1985; Mani 1989). This includes at least 30 species,
from 11 families in six orders, including Hemiptera,

Biological control of Maconellicoccus hirsutus 245
Table 3. Natural enemies introduced/considered for introduction into the Caribbean for control of
M. hirsutus
Natural enemy Procured from Agencies responsible
A. kamali China CABI Bioscience
Pakistan Hawaii USDA-APHIS subsequently obtained populations from
Pakistan and Hawaii
C. montrouzieri India CARDI/Ministry of Agriculture Land and Marine Resources,
Trinidad and Tobago
USA Many National programs imported CM from commercial
suppliers in USA
S. coccivora India CARDI/Ministry of Agriculture Land and
Marine Resources, Trinidad and Tobago
G. indica Egypt, Pakistan and
Australia
USDA-APHIS
A. dactylopii China CABI Bioscience
Neuroptera, Lepidoptera, Diptera and Coleoptera. The
parasitoid complex comprises at least 16 species
of parasitoids in six Hymenopteran families. The
most important species belong to the encyrtid genus
Anagyrus, notably A. kamali, A. dactylopii (Howard),
A. aegyptiacus Moursi and an unidentified species.
Another encyrtid, Leptomastix phenacocci Compere,
has also been reported as important. More recently,
G. indica was collected in Egypt, Pakistan and Australia
(USDA 1999). Among the predators, coccinellid
beetles are the most important. Species of particular
note include C. montrouzieri, S. coccivora, Scymnus
sp. nr. nubilis Mulsant, S. conformis Jordan and Brumoides
suturalis (F.). The natural enemy species that
have been introduced into the Caribbean or considered
for introduction are listed in Table 3 and these are discussed
below.
Parasitoids
Two parasitoids have been introduced and released
against HMB and these are A. kamali and G. indica.
A third parasitoid, A. dactylopii, was also considered
but was not introduced. A. kamali was the first natural
enemy to be introduced into the Caribbean for control
of HMB. The recommendations to introduce this
parasitoid were based on previous successful introduction
against HMB in Egypt (Kamal 1951). This was
supported by the fact that the fortuitous introduction
of A. kamali and another Anagyrus sp. was apparently
one of the reasons why HMB was not serious in
Hawaii (Beardsley 1985). In India, Anagyrus spp. were
also reported as important natural enemies of HMB
(Ghose 1971; Mani 1989). Finally, available information
showed that this parasitoid had a narrow host range
(Cross & Noyes 1995). The parasitoid was first released
in Grenada and subsequently to most of the affected
countries.
A. kamali is a solitary endo-parasitoid. Like many
encyrtids, adults also host feed and this may contribute
considerably to the overall mortality (Noyes & Hayat
1994). Moursi (1948) gives the earliest account on its
biology. Kairo et al. (1997) provide some details of its
development, particularly in relation to rearing. More
recent studies have concentrated on host stage preference,
host immune response and life table statistics
(Sagarra et al. 2000; Sagarra & Vincent 1999; Persad &
Khan (in press)).
G. indica was collected by USDA-APHIS in Egypt,
Pakistan and Australia and introduced initially to
St. Kitts. It has also now also been released in USVI,
Puerto Rico, Grenada, Belize and California. The parasitoid
reportedly became established in St. Kitts and
other locations, based on data from impact assessment
studies at several release sites (Meyerdirk 1999). There
is little information available on its biology beyond the
fact that it is a solitary endo-parasitoid.
Predators
Two predators were introduced for control of HMB,
C. montrouzieri and S. coccivora. Because of its wide
host range, C. montrouzieri has been used for control
of many other mealybug species including control
of HMB in Egypt and India (Bartlett 1978; Moore
1988). In Egypt, large numbers of C. montrouzieri
were released from 1922 but although it become established
it was not effective because of poor survival during
winter (Hall 1926). In India inoculative releases
of C. montrouzieri to control HMB on grapes have
been quite successful (Mani 1988). On this basis,
C. montrouzieri was selected for introduction. An area
of concern was its wide host range with the potential

246 M.T.K. Kairo et al.
for impacting on non-target organisms. However, the
pressure to control HMB rapidly negated serious consideration
of such concerns in many countries, at
least initially. In the Caribbean, C. montrouzieri has
been released widely and was particularly significant
in rapidly bringing down high populations. However,
as a high density feeder, its ability to maintain low
pest populations was considered to be limited. Indeed
there were concerns that the predator would become
extinct. It is noteworthy that although the predator was
previously introduced into several Caribbean islands
where it became established, for instance, in St. Kitts
(Cock 1985), it was apparently absent when HMB
was introduced. While there is potential for the predator
to be used against many mealybug species, its
use in the future may be limited because of concerns
about the potential negative impact on non-target
organisms.
C. montrouzieri has been widely studied. Accounts
of the developmental and reproductive biology are
given by Bhat et al. (1983), Satyanarayanamurthy and
Lakshmi Narayana (1986), Balakrishnan et al. (1987),
Mani and Thontadaraya (1987), Mani (1988), Gautam
(1996) and Kaufmann (1996). Mechanisms of host
location have been studied by Heidari and Copland
(1992 1993) and Merlin et al. (1996a,b). Both larvae
and adults of C. montrouzieri feed on the hosts
and detailed studies on consumption rates are reported
by Babu and Azam (1988), Mani (1988), Mani and
Thontadarya (1987), Oncuer and Bayhan (1982) and
Reddy et al. (1991).
Unlike C. montrouzieri, S. coccivora has no previous
history of successful introduction. The predator
was introduced into the USA from India in 1956 but
followup data are not available (Gordon 1985). The
species was also introduced from India to the Bahamas
for control of Pulvinaria maxima Green in 1956–57 but
did not become established (Cock 1985). S. coccivora
has been released in several countries in the Caribbean
for control of HMB including Trinidad and Tobago,
St. Kitts, British Virgin Islands and Grenada. Initial
indications suggested that it had become established
in some of the countries. However, subsequent studies
in Trinidad, where the most releases were made,
suggest that it is rare (Ramroop & Peterkin 1999). Its
contribution to HMB control has been minimal if at
all. Accounts of the developmental and reproductive
biology of S. coccivora are given by Gautam (1996),
Mani and Thontadarya (1987), Padmaja et al. (1995)
and Peterkin et al. (1998b).
Implementation of the Code of Conduct for
the Import and Release of Exotic
Biological Control Agents
Recent years have seen increased concerns over the
potential impact of introduced agents on non-target
species (Howarth 1991; Simberloff & Stiling 1996;
Thomas & Willis 1998). In 1996, the ‘Code of Conduct
for the Import and Release of Exotic Biological Control
Agents’ was ratified by FAO member countries
under the International Plant Protection Convention
(FAO 1996). The Code provides guidelines to be followed
when making introductions of natural enemies,
outlining the responsibilities of both exporting and
importing agencies. One of the requirements of the
Code is the production of a dossier containing information
on the host range, as well as risks associated
with introduction of any particular natural enemy. The
purpose of the dossier is to enable importing countries
to make an informed judgement on whether or
not to introduce a natural enemy. Dossiers were prepared
on all the natural enemies introduced under the
FAO funded projects. A dossier on A. kamali was first
prepared by Cross and Noyes (1995) and this was subsequently
revised by Kairo and Peterkin (1998). Similarly,
dossiers on C. montrouzieri and S. coccivora
were first prepared by Gautam and Parasram (1996a,b).
These were revised extensively by Peterkin et al.
(1998a,b) following additional studies and also to conform
more specifically to the Code. USDA-APHIS
prepared an Environmental Assessment (EA) prior to
introduction of A. kamali and G. indica in St. Kitts
(Meyerdirk 1997). This EA was prepared following US
regulations on import and release of exotic natural enemies
and served a similar purpose as the dossiers.
During the implementation of the work programme,
it was clear that most national programs did not have
specific mechanisms in place to regulate the introduction
of natural enemies. It is clear that there is an urgent
need for this to be addressed. Much still has to be done
to develop the framework for implementation of the
Code. There is a need to develop the necessary legal
framework and identify responsible authorities within
countries. It is essential for biological control practitioners
to foster implementation of the Code.
Natural enemy introductions into countries
Introduction and rearing natural enemies
Initial introductions of natural enemies were made
from several countries including China, Egypt, India,

Biological control of Maconellicoccus hirsutus 247
USA and UK. CABI Bioscience procured A. kamali
from China through collaboration with the Guangdong
Entomological Institute. Subsequently, USDA-APHIS
procured A. kamali from Hawaii. C. montrouzieri and
S. coccivora were initially sourced from India through
a collaborative programme between the Indian Agricultural
Research Institute (IARI), CARDI and the
Ministry of Agriculture Land and Marine Resources,
Trinidad and Tobago. Subsequent introductions were
made from commercial suppliers in USA and UK.
G. indica was procured from Egypt through the USDA-
APHIS programme. After the initial introductions,
natural enemies were supplied to countries by several
agencies and national programs as listed below:
(a) CABI Bioscience facilities in the UK and Trinidad
(A. kamali and S. coccivora).
(b) USDA-APHIS facilities in Newark and St. Thomas
(A. kamali and G. indica).
(c) National programs particularly in St. Kitts (in collaboration
with USDA-APHIS) and Trinidad and
Tobago (A. kamali, G. indica, C. montrouzieri and
S. coccivora).
(d) Commercial suppliers in the US and UK specifically
for C. montrouzieri.
Due to the lack of adequate facilities for rearing
natural enemies, many of the countries had to rely
entirely on supply of natural enemies from outside
sources. Quarantine of natural enemies within target
countries was not possible but specific measures were
taken to ensure that only clean material was introduced.
Under the CABI Bioscience programme, the
measures included a system of rigorous checks at each
stage of the rearing process to ensure that cultures were
clean. Additionally, only adult insects were shipped
thus allowing a final check to verify species identity.
The specific measures taken for each natural enemy
are detailed in the dossiers. Thus, it was possible for
countries to review the procedures in advance to satisfy
themselves that the shipments met their requirements.
It is assumed that other programmes supplying natural
enemies followed similar procedures. Exchange
of natural enemies between national programs was
possible following establishment of rearing facilities
in some of the countries. The techniques for rearing
natural enemies varied from complex systems, particularly
for the parasitoids, to simple systems involving
use of field collected host material as food, e.g.
for C. montrouzieri. Several laboratory rearing manuals
were developed (Gautam 1996; Kairo et al. 1997;
Meyerdirk et al. 1998).
Table 4 gives a list of natural enemies introduced
into different countries. A. kamali and C. montrouzieri
have been introduced into all the countries where the
pest is present. The other two natural enemies have
been introduced into only some of the countries.
Release strategies
In most cases, the species and numbers of natural enemies
released were dictated by availability. The choice
of release sites was based on location where infestations
occurred first. For instance, in most countries,
initial infestations of HMB were usually in urban areas
where mainly ornamentals and fruit trees were affected.
The distribution of such plants was often discontinuous
but this does not appear to have posed a problem
with the establishment of natural enemies. It is possible
that because of the wide host range of HMB, what
appeared as a discontinuous distribution was perhaps
fairly continuous allowing natural enemies to move
between affected plants.
Because of the distribution of affected plants in small
clumps, numbers of natural enemies released at each
site varied and was based on simple practical considerations.
For C. montrouzieri, releases comprised of a
few individuals per bush to several hundred in case of
large trees. In the case of A. kamali, releases varied
from about 50 per bush to several hundred per hedge
in the case of hibiscus or for large trees. Releases at
each site were usually in hundreds (Kairo et al. 1999).
However, it is important to note that overall the major
determinants of numbers released were availability and
size of pest population.
An important consideration was whether to separate
the releases of C. montrouzieri and A. kamali
both spatially and temporally. Apart from direct competition
for hosts, there was also the possibility that
C. montrouzieri would feed on parasitized mealybugs,
thus reducing the chances of establishment of the introduced
parasitoids. Therefore, where possible, efforts
were made to separate releases. In view of the suggestion
that C. montrouzieri is a high density feeder,
the predator was released first followed by A. kamali a
few weeks later. However, while no studies were conducted
to assess the effectiveness of this strategy, the
success of the approach, where implemented, indicates
its practical value.
An interesting component of the release programme
was the involvement of the public, particularly in
redistribution of C. montrouzieri (Stewart 1999). This
proved very effective in Trinidad and Tobago, and was
tried in some of the countries.

248 M.T.K. Kairo et al.
Table 4. Releases of four species of natural enemies by country
Country Natural enemy Date first Period over which Total released Result Reference
released releases made
Grenada A. kamali Oct. 1996 96–98 190,905 E Adrian Thomas
C. montrouzieri Apr. 1997 96–98 110,250 E unpubl. report
S. coccivora July 1998 98–99 (1925) ? Peters (1999)
G. indica 1998 98– 1500 ?
Trinidad and A. kamali Feb. 96 1Feb. 96–Oct. 96. 49,420 E Kairo et al. (1999)
Tobago C. montrouzieri Feb. 96 1Feb. 96–Oct. 96 14,861 E Gautam et al. (1999)
S. coccivora Feb. 96 1Feb. 96–Oct. 96 3740 ? Gautam et al. (1999)
G. indica Fortuitous introduction in Trinidad E Anon. (2000)
St. Kitts A. kamali Aug. 96 96–98 66,000 E Francis (1999)
C. montrouzieri 96 96–98 206,300 E
S. coccivora 96 96 Only 1300 N
G. indica 97 97–98 3200 E
St. Lucia A. kamali Jan. 97 97–98 E Anon. 1999a
C. montrouzieri Oct. 96 96–98 396,500 E
St. Vincent and A. kamali Nov. 97 97–98 28,000 E Edwards (1999)
the Grenadines C. montrouzieri Sep. 96 96–98 101,000 E
Guyana A. kamali July 1997 97–99 15,240 E Anon. (1999b)
C. montrouzieri May 1997 97– 56,000 E
US Virgin Islands – A. kamali June 1997 97–99 72,410 E Meyerdirk (1999)
St. Thomas, St. Croix, C. montrouzieri 45,000 E
St. John G. indica 60,240 E
British Virgin Islands A. kamali Jan. 1998 98 9500 E CABI Bioscience records
C. montrouzieri 98 18,300 E W. De Chi, personal
Communication
S. coccivora 98 250 Not est.
Montserrat A. kamali Dec. 1997 97–98 9250 ? CABI Bioscience, records
C. montrouzieri ? ? ? ?
Puerto Rico A. kamali May. 98 ? 1200 E Meyerdirk (1999)
G. indica Aug. 98 ? 2000 E
Culebra A. kamali Jan. 98 ? 1250 E
Vieques G. indica Apr. 98 ? 1500 E
Curaçao A. kamali Apr. 1999 99 7000 E CABI Bioscience, records
Anguilla A. kamali June 1999 99 2850 ? CABI Bioscience, records
Belize A. kamali Oct. 99 99–00 27,000 E Anon. (2000)
C. montrouzieri Oct. 99 20,000 E
G. indica Nov. 99 5800 E
USA, California A. kamali 99 Ongoing ? ? D. Meyerdirk,
personal Communication
G. indica 99 Ongoing ? ?
C. montrouzieri 99 Ongoing ? ?
1 Denotes period of intensive release, small releases were being made up to 1999. Other countries which have also released natural
enemies but for which data was not available include: The Netherlands Antilles (St. Eustatius and Aruba), French Antilles (Guadeloupe,
Martinique, St. Martin) and Nevis.
The period over which releases were made depended
on the availability of natural enemies and concerns
over apparent upsurges of the pest, particularly in
the dry season. Thus in cases where countries had
the capability to rear natural enemies, releases were
continued over several years, particularly in Grenada,
and Trinidad and Tobago. The value of the extended
release period is debatable, as countries which made
releases over specific time periods such as St. Lucia
and St. Kitts achieved similar levels of control.
Prophylactic releases
The possibility of making ‘prophylactic releases’, that
is the pre-emptive release of natural enemies as a

Biological control of Maconellicoccus hirsutus 249
preventative measure, was considered in some of the
affected countries. For obvious reasons the strategy
was only possible for a generalist natural enemy such
as C. montrouzieri which could survive on other hosts.
Towards this end, the predator was released in Barbados
and Dominica. While Dominica and Barbados have
only recently become affected, this cannot be attributed
to the prophylactic releases. It should be noted that
the chances of even such a generalist natural enemy
becoming established are small since most potential
hosts are likely to be rare, being themselves under
good natural control. Indeed anecdotal evidence from
Barbados suggests that the released material may have
died out (Lennox Chandler, personal communication).
Therefore, as yet, there is no evidence to the authors’
knowledge where such releases have been effective. In
view of the concerns over possible impact on non-target
organisms by generalist natural enemies, it is unlikely
that such a strategy will be of practical value in future
biological control programmes.
Establishment and impact of natural enemies
A. kamali, C. montrouzieri and G. indica became
established in all countries where they were released
(Table 3). However, although recovered a few months
after release, there is little evidence to show that
S. coccivora became established, even in Trinidad
where most of releases were made. Interestingly,
A. kamali and G. indica appear to have become fortuitously
introduced into at least two islands, Curaçao
and Trinidad, respectively. The appearance of G. indica
in Trinidad in 1999 was intriguing, as the majority of
releases of the parasitoid had been made in the northern
Caribbean. It would seem to suggest that mealybug
infested material was still getting into Trinidad (Anon.
2000). Of particular note was the difficulty in getting
establishment of both A. kamali and C. montrouzieri
on blue mahoe in the Grand Etang area in Grenada.
Despite repeated releases of these natural enemies in
this area, recoveries were always very poor. Interestingly,
populations of HMB on this tree appear to
have diminished anyway, possibly due to plant related
factors.
The type of studies carried out to assess impact of
natural enemies varied considerably from country to
country. Countrywide surveys were conducted in several
countries notably Grenada, Trinidad and Tobago,
St. Vincent and the Grenadines, and Guyana but the
results have not been published. In the US territories,
and St. Kitts and Nevis, population counts were made
at specific sites mainly by sampling hibiscus. These
have shown a distinct and significant role of A. kamali
in controlling HMB (Meyerdirk 1999).
Detailed studies were carried out to quantify population
growth parameters of A. kamali, C. montrouzieri
and S. coccivora under laboratory conditions (Persad
1999). Under field conditions, C. montrouzieri was
very effective in reducing HMB populations and this
was demonstrated by McComie et al. (1999). Studies
carried out by Meyerdirk (1997) in the northern
Caribbean, appear to support the notion that A. kamali
is particularly important in maintaining low densities
of the pest. At the outset, there was doubt as to whether
C. montrouzieri, a high density predator, would persist
when HMB populations became low. There is evidence
which shows that it has in actual fact continued to persist
in the field two years after introduction in some
of the countries. Whether or not it will persist in the
long term remains to be seen. No studies have been
carried out under field conditions to compare the relative
contribution of each of the introduced natural enemies.
However, there is some evidence suggesting that
A. kamali may displace G. indica under field conditions
(Meyerdirk, personal communication).
The current status
A regional workshop was organized at the conclusion
of the FAO project in March 1999 to assess the progress
with the biological control programme (Anon. 1999c).
It is quite clear that in all the countries where biological
control has been implemented, this has resulted in very
good control. However concerns about the effectiveness
of control on certain crops have been expressed
(Peters 1999). The most notable are soursop (Annona
muricata) and sorrel (Hibiscus sabdarifa). Populations
of the pest apparently build up to high levels before
natural enemies can bring them under control. There
is a need for detailed studies to understand the population
dynamics of the pest and natural enemies on
these crops, in order to determine how serious the
problem is and to identify windows of opportunity for
intervention.
Factors leading to rapid success with biological
control of HMB in the Caribbean
Because natural enemies of HMB were already known,
it was possible to make arrangements for their supply
to the Caribbean within a short space of time. For
instance, CABI Bioscience linked with collaborators
in China who supplied the initial stocks of A. kamali.

250 M.T.K. Kairo et al.
Similarly, through links with the IARI, CARDI was
able to obtain initial stocks of C. montrouzieri and
S. coccivora for subsequent release and rearing. However,
once an inexpensive source of C. montrouzieri
was identified from commercial sources in the United
States of America, the predator was subsequently procured
by many national programs from this source.
Through the regional FAO funded project all countries,
including non-beneficiary ones, were supplied
with natural enemies, particularly A. kamali, when
requested. There was tremendous goodwill and collaboration
between national programs, regional and international
organizations towards the biological control
effort.
Because many ornamental plants, home gardens and
field crops were affected, the wider population had a
great interest in the control of HMB. Effective public
awareness programmes ensured cooperation. Thus
adverse measures such as indiscriminate spraying with
chemical pesticides or removal of plants which could
have negatively affected the biological control effort
were avoided. In Trinidad and Tobago, and other countries,
the public also played a key role in redistribution
of the biological control agents, particularly
C. montrouzieri.
Following the extensive devastation in Grenada,
regional governments recognized the danger posed by
the pest and allocated resources towards the management
of the pest. The response of international
organizations/funding agencies, most notably FAO, in
supporting a regional biological control effort was crucial
to the success achieved. Clearly, the need for a rapid
reaction capability such as that provided by the FAO
Technical Cooperation Programme is vital to facilitate
quick action to deal with new invasive pests that can be
targeted for biological control.
Benefits from the programme
Apart from economic benefits, the programme also
contributed to safeguarding both environmental and
human health. It also resulted in development of capacity
to undertake biological control programmes. More
importantly, it has set the scene for implementation of
integrated pest management. These benefits are discussed
in greater detail below.
The economic benefits derived from successful control
of HMB were enormous. One only needs to consider
the estimated losses (above) to appreciate this.
While there is a limited amount of detailed ecological
data on the impact of natural enemies, for
most countries, this was purely an academic question.
Results of control were seen in renewed production of
those crops that had been particularly badly affected
such as annonas (Annona spp.), plums (Spondias
spp.), sorrel (Hibiscus sabdariffa), okra (Abelmoschus
esculentus) etc. Ornamental hibiscus is once again
flourishing, whereas there was a time when flowering
hibiscus shrubs were rare. More importantly, trade
between infested and uninfested countries has been
resumed to some extent, following the development of
export protocols.
Severe devastation of natural habitats as seen, for
example, in the Grand Etang area in Grenada where
a stand of 38 ha of blue mahoe (Hibiscus elatus)
was destroyed, has now been averted elsewhere. For
small island states, such severe damage has potentially
serious long-term effects. Furthermore, there
is no doubt that continued application of chemical
pesticides would have been harmful to humans and
the environment.
Many of the affected countries in the Caribbean
were ill-prepared to mount a classical biological control
project. With few exceptions there was a general lack
of trained personnel and insect rearing facilities. However
several countries established rearing facilities, for
instance, Grenada, Guyana, St. Kitts and Nevis, and
Trinidad and Tobago. Similarly several training courses
were held and staff were attached to laboratories rearing
natural enemies. Suffice to say that there is now a
cadre of trained personnel in most countries, able to
implement a biological control programme.
One of the important benefits of the project is that
it established in the minds of many stakeholders –
farmers, policy makers and politicians, householders
etc. – that biological control is a viable alternative to
chemical pest control and a practical solution to some
pest problems. This has provided good publicity for
biological control which can only make it easier to promote
as a component of IPM programmes.
Quarantine, pest detection and identification
The importance of quarantine in preventing the introduction
of exotic pests can not be over-emphasized.
The first step in dealing with any invasive pest is
timely detection and correct identification. The initial
invasion of HMB in Grenada probably went undetected
for two years. The reasons for this are not clear
but by the time the pest was identified, it had spread
throughout Grenada. Experiences in other countries
that became affected subsequently, showed that early

Biological control of Maconellicoccus hirsutus 251
implementation of biological control slowed spread of
the pest and substantially curtailed damage. Thus, it
is vital for countries to institute mechanisms to allow
early detection of exotic pests. While correct identifications
were made in the case of HMB, it is important to
note that the literature has several spectacular examples
where incorrect identification of the pests hindered and
slowed implementation of biological control. Furthermore,
the presence of a pest may have serious implications
for trade. Greater emphasis will need to be placed
in future on the development of skilled personnel and
in the allocation of necessary resources to ensure that
effective quarantine measures are implemented.
Future opportunities
Mealybugs and indeed other Homoptera are easily
transported on plant material and the danger of new
introductions is ever present. Clearly, not all introduced
species have become serious pests and there are many
possible reasons for this. For instance, some of the
species may have been introduced with their natural
enemies. There are several examples of this happening
but perhaps most relevant is the case of HMB in
Hawaii (Beardsley 1985), and in Trinidad and Curaçao
(cited above). It is also possible that indigenous natural
enemies may adapt to effectively suppress populations
of the invading species. It would be expected
that that mealybug species with restricted host range
are less likely to become apparent when introduced,
particularly if their hosts are not widespread or of economic
importance. Indeed a polyphagous species has
a far greater chance of becoming established in a new
locality. Clearly not all introduced species will require
intervention. However, at present, at least one exotic
mealybug species, Paracoccus marginatus Williams &
Granara de Willink is spreading through the Caribbean
and requires urgent attention.
Conclusions
The speed with which HMB spread through the
Caribbean is remarkable. A number of factors responsible
for this are identified. The biological control programme
against the pest has been a tremendous success
and the speed with which positive results were achieved
is remarkable. The success is mainly attributable to the
two natural enemies, A. kamali and C. montrouzieri.
The programme provided an excellent opportunity to
implement the code of conduct for the introduction
and release of exotic natural enemies, a significant step
forward in the implementation of arthropod pest control.
The programme for control of HMB has served to
develop capacity in biological control and taxonomic
skills within Caribbean national systems and also to
popularize biological control in the widest sense.
Scientifically, it is interesting in that both generalist
and specialist natural enemies were used. Although
there is a limited amount of ecological information, it
is clear that A. kamali alone can control the pest but
this takes a longer period. Thus although the generalist
predator, C. montrouzieri may give a rapid reduction
of pest populations, its introduction can be avoided
if A. kamali is introduced early. However, there is a
dearth of empirical data on ecological assessment of the
impact of these natural enemies. Particular areas of
interest would be the relative contribution of each of
the natural enemies to the control achieved. The apparent
persistence of C. montrouzieri is worthy of further
study as well as the impact of these natural enemies on
non-target organisms. Because of the possibility of conducting
comparative studies on the different islands, the
Caribbean would be ideal for carrying out such studies.
Further research is also needed to develop ways
of enhancing the effectiveness of natural enemies in
some cropping systems notably on soursop and to a
lesser extend on sorrel.
Acknowledgements
We wish to thank, several persons for sharing
information and commenting on the manuscript, Dale
Meyerdirk, Lennox Chandler and Matthew Cock.
References cited
Anonymous (2000) Parasitoids island hop too. Biocontrol News
Inform. 21, 27N–29N.
Anonymous (1999a) Summary of activities associated with
Maconellicoccus hirsutus in St. Lucia. Paper presented at
the Evaluation Workshop on Biological Control of Hibiscus
Mealybug, Maconellicoccus hirsutus in the Caribbean Sub
Region, 11–12 March 1999, Trinidad and Tobago.
Anonymous (1999b) The pink mealybug (Maconellicoccus
hirsutus) in Guyana. Country Report. Paper presented at
the Evaluation Workshop on Biological Control of Hibiscus
Mealybug, Maconellicoccus hirsutus in the Caribbean Sub
Region, 11–12 March 1999, Trinidad and Tobago.
Anonymous (1999c) Report on the Evaluation Workshop on
Biological Control of Hibiscus Mealybug, Maconellicoccus
hirsutus in the Caribbean Sub Region, FAO unpublished report,
11–12 March 1999, 23 pp. Trinidad and Tobago.

252 M.T.K. Kairo et al.
Babu, T.R. & Azam K.M. (1988b) Predation potential of
Cryptolaemus montrouzieri Mulsant (Coccinellidae: Coleoptera)
in relation to temperature. J. Res. APAU 16, 108–10.
Balakrishnan, M.M., Kumar, P.K.V. and Govindarajan, T.S.
(1987) Cryptolaemus montrouzieri: comparison of life cycle
on Chloropulvinaria psidii and Planococcus citri. J. Coffee
Res. 17, 59–61.
Bartlett, B.B. (1978) Pseudococcidae. In C.P. Clausen (ed)
Introduced Parasites and Predators of Arthropod Pests and
Weeds: A World Review, pp. 137–70. United States Department
of Agriculture Handbook No. 480.
Beardsley, J.W. (1985) Notes and Exhibitions. Proc. Hawaiian
Entomol. Soc. 25, 27–8.
Bhat, P.K., Chacko, M.J., Sreedharan, K. and Venkata Ram, C.S.
(1983) Biology of the ladybird beetle, Cryptolaemus
montrouzieri Mulsant, a predator of mealybugs. In C.S. Venkata
Ram (ed) Proc. Sec. Ann. Symp. Plant. Crops. Plant protection
(entomology, microbiology, nematology, plant pathology and
rodentology). PLACROSYM II 1979, pp. 221–6. Kerala, India.
Cock, M.J.W. (1985) A review of biological control of pests in the
Commonwealth Caribbean and Bermuda up to 1982. Technical
Communication No. 9, 218 pp. Commonwealth Institute of
Biological Control.
Cross, A.E. and Noyes, J.S. (1995) Dossier on Anagyrus kamali
Moursi Biological Control Agent for the Pink Mealybug,
Maconellicoccus hirsutus, in Trinidad, 17 pp. Ascot: International
Institute of Biological Control.
Edwards, S. (1999) Biological control of the pink mealybug
(Maconellicoccus hirsutus) in St. Vincent and the Grenadines
1996–1998. Paper presented at the Evaluation Workshop on
Biological Control of Hibiscus Mealybug, Maconellicoccus
hirsutus in the Caribbean Sub Region, 11–12 March 1999,
Trinidad and Tobago.
FAO (1996) Code of conduct for the import and release of exotic
biological control agents, 14 pp. Rome: Food and Agricultural
Organization of the United Nations.
Francis, A. (1999) Report on biological control activities (pink
hibiscus mealybug), St. Kitts. Paper presented at the Evaluation
Workshop on Biological Control of Hibiscus Mealybug,
Maconellicoccus hirsutus in the Caribbean Sub Region, 11–12
March 1999. Trinidad and Tobago.
Francois, B. (1996) Measuring the impact of mealybug infestation.
Proceedings of the First Symposium on the Hibiscus
Mealybug in the Caribbean, 24–27 June 1996, Grenada.
Gautam, R.D. (1996) Multiplication and use of exotic coccinellids
– a manual, 30 pp. Trinidad and Tobago: Caribbean
Agricultural Research and Development Institute.
Gautam, R.D. and Parasram, S. (1996a) Dossier on Cryptolaemus
montrouzieri Mulsant, Biological Control Agent for the
Hibiscus Mealybug, Maconellicoccus hirsutus (Green) in
Trinidad and Tobago, West Indies. Unpublished Report, 12 pp.
Caribbean Agricultural Research and Development Institute.
Gautam, R.D. and Parasram, S. (1996b) Dossier on Scymnus
coccivora Ayyar, Biological Control agent for the Hibiscus
Mealybug, Maconellicoccus hirsutus (Green) in Trinidad and
Tobago, West Indies. Unpublished Report, 10 pp. Caribbean
Agricultural Research and Development Institute.
Gautam, R.D., DeChi, W. and Maraj, C. (1999) Impact of
Cryptolaemus montrouzieri Mulsant and Scymnus coccivora
Aiyar in controlling the hibiscus mealybug, Maconellicoccus
hirsutus (Green) in Trinidad. Proc. 1st Sem. Hibiscus
Mealybug, 12 April 1996, Farmers’ Training Centre, Centeno,
Trinidad and Tobago, Ministry of Agriculture, Land and Marine
Resources.
Gautam, R.D., Pilgrim, R.N. and Stewart, V. (2000) Protocols
for the protection of agricultural production and trade, 53 pp.
Trinidad and Tobago: Caribbean Agricultural Research and
Development Institute.
Ghose, S.K. (1970) Predators, parasites and attending ants of
the mealybug, Maconellicoccus hirsutus (Green) (Pseudococcidae,
Hemiptera). Plant Prot. Bull, India 22, 22–30.
Ghose, S.K. (1971) Chemical control of the mealybug, Maconellicoccus
hirsutus (Green) (Pseudococcidae: Homoptera). Plant
Prot. Bull, India 22, 17–21.
Gordon, R.D. (1985) The Coccinellidae (Coleoptera) of America
North of Mexico. J. New York Entomol. Soc. 93, 901–912.
Hall, W.J. (1926) The hibiscus mealy bug (Phenacoccus hirsutus,
Green) in Egypt in 1925 with notes on the introduction of
Cryptolaemus montrouzieri, Muls. Bulletin of the Ministry of
Agriculture, Egypt Technical and Scientific Services No. 70.
15 pp.
Heidari, M. and Copland, M.J.W. (1992) Host finding by
Cryptolaemus montrouzieri (Col., Coccinellidae) a predator of
mealybugs (Hom., Pseudococcidae). Entomophaga 37, 621–5.
Heidari, M. and Copland, M.J.W. (1993) Honeydew: a food
source or arrestant for the mealybug predator, Cryptolaemus
montrouzieri? Entomophaga 38, 63–8.
Howarth, F.G. (1991) Environmental impacts of classical biological
control. Ann. Rev. Entomol. 36, 485–509.
IICA (1999) Facilitation of Caribbean intra-regional trade in
fresh produce. Technical Cooperation Agency, March 1999.
Barbados, Areas of concentration III: Agricultural Health.
IIE (International Institute of Entomology) (1997) Maconellicoccus
hirsutus. Distribution Maps of Pests, Series A
(Agricultural), Map No. 100 (second revision), 4 pp.
Kairo, M.T.K. (1997) Assessment of the biological control programme
for the Hibiscus Mealybug, Maconellicoccus hirsutus
(Green) in Grenada. Report on a consultancy mission to
Grenada under TCP/RLA/6719: Assistance for Biological Control
of the Pink Mealybug: Technical Report, 27 pp. Trinidad
and Tobago: CABI Bioscience.
Kairo, M.T.K. and Peterkin, D.D. (1998) Dossier on Anagyrus
kamali Moursi (Hymenoptera: Encyrtidae), a Potential
Biological Control Agent for the Hibiscus Mealybug, Maconellicoccus
hirsutus (Green) in the Caribbean, 34 pp. Trinidad
and Tobago: CABI Bioscience, Caribbean and Latin American
Centre.
Kairo, M.T.K., Morais, M. and Cooper, B. (1999) Field release
and establishment of Anagyrus kamali Moursi (Hymenoptera:
Encyrtidae), a parasitoid of the hibiscus mealybug, Maconellicoccus
hirsutus (Green) (Homoptera: Pseudococcidae) in
Trinidad. In Proc. 1st Sem. Hibiscus Mealybug, 12 April 1996,
pp. 44-54. Farmers’ Training Centre, Centeno, Trinidad and
Tobago, Ministry of Agriculture, Land and Marine Resources.
Kairo, M.T.K., Cross, A.E., Lopez, V.F., Peterkin, D.D. and
Ram, P. (1997) Biological Control of the Hibiscus Mealybug:
Rearing the Hibiscus Mealybug, Maconellicoccus Hirsutus
(Green) and the Parasitoid, Anagyrus kamali Moursi, 33pp.
Trinidad: International Institute of Biological Control.
Kamal, M. (1951) Biological control projects in Egypt, with a list
of introduced parasites and predators. Bulletin de la Société
Fouad Ier d’Entomologie 35, 205–20.

Biological control of Maconellicoccus hirsutus 253
Kaufmann, T. (1996) Dynamics of sperm transfer, mixing,
and fertilization in Cryptolaemus montrouzieri (Coleoptera:
Coccinellidae) in Kenya. Ann. Entomol. Soc. Ame. 89, 238–42.
Mani M. (1988) Bioecology and management of grapevine
mealybug. Technical Bulletin No. 5, 32 pp. Indian Institute of
Horticultural Research.
Mani, M. (1989) A review of the hibiscus mealybug – Maconellicoccus
hirsutus (Green). Ins. Sci. Appl. 10, 157–67.
Mani, M. and Thontadarya, T.S. (1987) Development and feeding
potential of coccinellid predator, Cryptolaemus montrouzieri
Muls. on the grape mealybug, Maconellicoccus hirsutus
(Green). J. Biol. Cont. 1, 19–22.
McComie, L.D. (1997) Incidence and treatment of the hibiscus
mealybug Maconellicoccus hirsutus (Green) August 1995 –
February 1996. In Proc. 1st Sem. Hibiscus Mealybug, 12 April
1996, pp. 59–77. Farmers’ Training Centre, Centeno, Trinidad
and Tobago, Ministry of Agriculture, Land and Marine
Resources.
McComie, L.D., Gosine, S. and Siew, P. (1999) The population
dynamics of Maconellicoccus hirsutus (Green) (Homoptera:
Pseudococcidae) in relation to rainfall and management of
the mealybug in Trinidad. Paper presented at the Evaluation
Workshop on the Biological Control of the Pink Hibiscus
Mealybug, Maconellicoccus hirsutus, in the Caribbean Subregion.,
11–12 March 1999, 8 pp. Port of Spain, Trinidad and
Tobago.
Merlin, J., Lemaitre, O. and Gregoire, J.C. (1996a) Oviposition
in Cryptolaemus montrouzieri stimulated by wax filaments of
its prey. Entomologia Experimentalis et Applicata 79, 141–6.
Merlin, J., Lemaitre, O. and Gregoire, J.C. (1996b) Chemical
cues produced by conspecific larvae deter oviposition by the
coccidophagous ladybird beetle, Cryptolaemus montrouzieri.
Entomologia Experimentalis et Applicata 79, 147–51.
Meyerdirk, D.E. (1999) Pre-emptive thrust against the pink hibiscus
mealybug – a model for meeting invasive threats in the
Caribbean. Paper presented in a Workshop on Approaches to
Mitigating the Effects of Exotic Pests on Trade and Agriculture
in the Caribbean Region, 16-18 June 1999. Caribbean Basin
Administrative Group, Homestead, FL.
Meyerdirk, D.E. (1997) Field Releases of Nonindigenous Species
of Anagyrus and Gyranusoidea (Hymenoptera: Encyrtidae) for
Biological Control of Pink Hibiscus Mealybug, Maconellicoccus
Hirsutus (Homoptera: Pseudococcidae): Environmental
Assessment, 16 pp. United States Department of Agriculture.
Meyerdirk, D.E., Warkentin, R., Attavian, B., Gersabeck, E.,
Francis, A., Adams, M. and Francis, G. (1998) Biological
Control of the Pink Hibiscus Mealybug Project Manual. United
States Department of Agriculture.
Moffitt, L.J. (1999) Economic risk to United States Agriculture of
Pink Hibiscus Mealybug invasion, 15 pp. Report to the Animal
and Plant Health Inspection Service, United States Department
of Agriculture.
Moore, D. (1988) Agents used for biological control of mealybugs
(Pseudococcidae). Biocontrol News Infor. 9, 209–25.
Moursi, M. (1948) Description of two new species of Anagyrus
(Hymenoptera: Encyrtidae). Bulletin de al Societe Fouad 1er
Entomology 32, 1–7.
Noyes, J.S. and Hayat, M. (1994) Oriental mealybug parasitoids
of the Anagyrini (Hymenoptera: Encyrtidae). CAB
International, Wallingford, UK.
Oncuer, C. and Bayhan, N. (1982) An investigation into the feeding
capacity and diet of Cryptolaemus montrouzieri (Muls.).
Turkiye Bitki Koruma Dergisi 6, 85–90.
Padmaja, C., Babu, T.R., Reddy, D.D.R. and Siramulu, M. (1995)
The biology and predation potential of Scymnus coccivora
Aiyar (Coleoptera: Coccinellidae) on mealybugs. J. Entomol.
Res. 19, 79–81.
Peterkin, D., Kairo, M.T.K. and Gautam, R.D. (1998a) Dossier
on Cryptolaemus montrouzieri (Mulsant) (Coccinellidae;
Scymninae), a Potential Biological Control Agent for the
Hibiscus Mealybug, Maconellicoccus hirsutus (Green) in the
Caribbean, 38 pp. Trinidad and Tobago: CABI Bioscience,
Caribbean and Latin American Centre.
Peterkin, D., Kairo, M.T.K. and Gautam, R.D. (1998b) Dossier
on Scymnus coccivora (Ramakrishna Ayyar) (Coccinellidae;
Scymninae), a Potential Biological Control Agent for the
Hibiscus Mealybug, Maconellicoccus hirsutus (Green) in the
Caribbean, 34 pp. Trinidad and Tobago: CABI Bioscience,
Caribbean and Latin American Centre.
Peters, T. (1999) The pink mealybug (Maconellicoccus hirsutus)
in Grenada. Paper presented at the Evaluation Workshop on
Biological Control of Hibiscus Mealybug, Maconellicoccus
hirsutus in the Caribbean Sub Region, 11–12 March 1999,
Trinidad and Tobago.
Persad, A. (1999) Bioecological studies on Maconellicocus
hirsutus (Green) and its natural enemies, Anagyrus kamali
Moursi, Cryptolaemus montrouzieri (Mulsant) and Scymnus
coccivora (Ayyar). Unpublished Ph.D. Thesis, University of
the West Indies.
Persad, A. and Khan, A. (in press) Comparison of lifetable
parameters for Maconellicoccus hirsutus, Anagyrus kamali and
Scymnus coccivora. BioControl (in press).
PMC (Programme Management Committee) (1996) Regional
Action Programme for the Control of Pink Mealybug, Maconellicoccus
hirsutus (Green) in the Caribbean. Main report.
Presented at the Meeting of the Programme Coordinating
Committee, St. Kitts and Nevis, 26 February 1996, 57 pp.
Pollard, G.V. (1998) Update on New Pest Introductions, 11pp.
Circular letter No. 3/98, Food and Agricultural Organisation of
the United Nations (FAO) Regional Office for Latin America.
Pollard, G.V. (1997) Introduction and establishment of the pink
mealybug, Maconellicoccus hirsutus, in the Caribbean Subregion
and implications in the agriculture and forestry subsectors.
In C. Yocum and A.E. Lugo (eds) Protected areas
management: Proceedings of the Eighth Meeting of Caribbean
foresters, 3–7 June 1996, pp. 118–124. Institute of Tropical
Forestry, United States Department of Agriculture, Forest
Service, Rio Pedras, Puerto Rico.
Ramroop and Peterkin (1999) Biology, field release and evaluation
of Scymnus coccivora Ayyar (Coleoptera: Coccinellidae)
for biocontrol of Maconellicoccus hirsutus (Green) (Homoptera:
Pseudococcidae) in Trinidad and Tobago. Paper presented at
the Evaluation Workshop on Biological Control of Hibiscus
Mealybug, Maconellicoccus hirsutus in the Caribbean
Sub Region, 11–12 March 1999, 8 pp. Trinidad and
Tobago.
Reddy, K.B., Sreedharan, K. and Bhat, P.K. (1991) Effect of rate
of prey, Planococcus citri (Risso) on the fecundity of mealybug
predator, Cryptolaemus montrouzieri Mulsant. J. Coffee Res.
21, 149–50.

254 M.T.K. Kairo et al.
Sagarra, L.A., Peterkin, D.D., Vincent, C. and Stewart, R.K.
(2000) Immune response of the hibiscus mealybug, Maconellicoccus
hirsutus Green (Homoptera: Pseudoccidae), to
oviposition of the parasitoid Anagyrus kamali Moursi
(Hymenoptera: Encyrtidae). J. Ins. Physiol. 46, 647–53.
Sagarra, L.A. and Peterkin, D.D. (1999) Invasion of the Caribbean
by the hibiscus mealybug, Maconellicoccus hirsutus Green
(Homoptera: Pseudoccidae). Phytoprotection 80, 103–13.
Sagarra, L.A. and Vincent, C. (1999) Influence of host stage on
oviposition, development, sex ratio and survival of Anagyrus
kamali Moursi (Hymenoptera: Encyrtidae), a parasitoid of
the hibiscus mealybug, Maconellicoccus hirsutus Green
(Homoptera: Pseudocccidae). Biol. Control 15, 51–56.
Satyanarayanamurthy, M. and Lakshmi Narayana, K. (1986)
Biology of Cryptolaemus montrouzieri Muls. (Coleoptera:
Coccinellidae), a predatory beetle of mealybugs. Ind. Grape
J. 2, 40–52.
Simberloff, D. and Stiling, P. (1996) How risky is biological
control? Ecology 77, 1965–74.
Singh, R. (1999) Socio-economic impact and evaluation of the
HMB control programme. Paper presented at the Evaluation
Workshop on Biological Control of Hibiscus Mealybug,
Maconellicoccus hirsutus in the Caribbean Sub Region,
11–12 March 1999, Trinidad and Tobago.
Stewart, V. (1999) Public awareness as a strategy in the introductions
and/or infestations of the pink hibiscus mealybug.
Paper presented at the Evaluation Workshop on Biological
Control of Hibiscus Mealybug, Maconellicoccus hirsutus in
the Caribbean Sub Region, 11–12 March 1999, Trinidad and
Tobago.
Stibick, J.N.L. (1997) Pink Hibiscus Mealybg, New Pest
Response Guidelines, 104 pp. United States Department of
Agriculture.
Thomas, M.B. and Willis, A.J. (1998) Biocontrol – risky but
necessary? Trends Ecol. Evol. 13, 325–329.
United States Department of Agriculture (1999) Status Report:
4 March, 1999, Pink Hibiscus Mealybug Biological Control
Program in the United States Department of Agriculture
(USDA), 2 pp.
Williams, D.J. (1996) A brief account of the hibiscus mealybug
Maconellicoccus hirsutus (Hemiptera: Pseudoccocidae),
a pest of agriculture and horticulture, with descriptions of two
related species from southern Asia. Bull. Entomol. Res. 86,
617–28.
Williams, D.J. and Granara de Willink, M.C.G. (1992) Mealybugs
of Central and South America. Wallingford, UK: CAB
International. 635 pp.
Watson, G.W. and Chandler, L.R. (1999) Manual on the
identification of mealybugs important in the Caribbean region.
Commonwealth Science Council and CAB International.
Watson, G.W. and Chandler, L.R. (2000) Identificacion de
cochinillas o piojos harinosos de importancia en el Caribe
(translated by Marco Gaiani). Commonwealth Science Council
and CAB International.