Integrated Pest Management Reviews 5: 241–254, 2000. © 2001 Kluwer Academic Publishers. Printed in the Netherlands.

Biological control of the , hirsutus Green (: Pseudococcidae) in the

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: [email protected])

Accepted in final form 16 July 2001

Key words: biological control, , 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 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 involved and more natural enemies were introduced, most notably Cryptolaemus montrouzieri Mulsant The hibiscus mealybug (HMB), Maconellicoccus (Coleoptera: ). What happened next was hirsutus Green (Hemiptera: Pseudococcidae) was acci- the dream of any biological control practitioner. Within dentally introduced into the Caribbean in the early a short space of time pest populations were brought 1990s. It was first reported in Grenada in 1994 under control and the results were replicated in each after which it rapidly spread through countries in the country which became infested. With few exceptions Caribbean, becoming one of the most important pest much of the information arising from this programme species. Initial measures to control the pest using chem- has only been reported in local or regional publications. ical and cultural measures were costly, difficult to This paper gives an account of the pest with particular implement and/or ineffective (Pollard 1997; Sagarra & emphasis on the biological control effort. Peterkin 1999). As an exotic pest, HMB was a good tar- get for classical biological control and efforts to achieve this were initiated in 1995 in Grenada through a Tech- Origin, distribution and spread nical Cooperation Project of the Food and Agriculture Organization (FAO) of the United Nations and exe- HMB is native to parts of (Williams 1996). Prior to cuted by CABI Bioscience. This led to the introduc- its appearance in the Caribbean, the pest was known to tion of the endo-parasitoid Anagyrus kamali Moursi have a wide distribution in parts of Asia and (IIE (: ). Subsequently, and as the 1997). However, it had only ever been reported as a seri- pest spread to other countries, other agencies became ous pest in Egypt and . The only previous record of 242 M.T.K. Kairo et al. the pest in the New World is from Hawaii in 1983. How- useful in planning for similar situations in future. These ever, in stark contrast to the situation in the Caribbean, it factors are listed below: never became serious presumably because natural ene- (a) frequent movement of people and goods fostered mies were fortuitously introduced with it (Beardsley by close intra-regional economic and cultural link- 1985). Between 1994 and the present, the pest has ages, spread to over 25 territories in the Caribbean Basin, (b) as with other plant sucking and scales, from Guyana and Venezuela in the south to Bahamas in intimate association with its host plants increased the north and Belize and California in the west. Table 1 chances of spread through movement of plant gives the distribution of M. hirsutus in the region up to material, June 2001. (c) wide host range including many agricultural crops The pest appears to be inadvertently spread by as well as ornamentals which were frequently human beings. The rapid spread within the region was moved between the territories, remarkable, considering that many of the territories are (d) first instar nymphs and ovisacs could be easily islands. It is envisaged that an understanding of the key moved on passenger clothing, factors that may have led to this rapid spread would be (e) short distances between territories, thus chances that may easily survive the journey were Table 1. Distribution of M. hirsutus in the Caribbean high, and adjacent regions (f) quarantine was difficult for a pest with such a wide Country Date of reporting host range and furthermore, quarantine services Grenada and Carriacou November 1994 were (and continue to be) under-resourced in many Trinidad and Tobago August 1995/ November 1996 of the countries, St. Kitts and Nevis November 1995/ (g) existence of a thriving informal trade between December 1995 some of the islands which was difficult to police Netherlands Antilles from a quarantine perspective, Aruba ? (h) the public seemingly unaware of the risks posed by Sint Maarten September 1996 St. Eustatius May 1997 the pest and was thus likely to move plant material Curaçao June 1997 between different territories, Saint Lucia October 1996 (i) the fact that the pest may have remained uniden- Anguilla 1996?/February 1997 tified for some time in Grenada led to build up of Guyana April 1997 very high populations which increased the chances British Virgin Islands May 1997 (Tortola) of accidental movement. St. Vincent and May 1997 the Grenadines United States Virgin Islands Feeding and damage symptoms St. Thomas May 1997 St. John May 1997 HMB attacks new flush growth, young shoots, flowers St. Croix June 1997 and fruits. Both nymphs and female adults cause direct Montserrat January 1998 damage by sucking plant sap from the phloem. While Guadeloupe April 1998 feeding, HMB injects the plant with its toxic saliva, Puerto Rico which causes growth malformation characterized by Culebra December 1997 Vieques June 1997 curling and crinkling of leaves. These are usually some PR Mainland April 1998 of the first noticeable symptoms of HMB presence. USA: California August 1999 Continued feeding causes stunting, with shortening (Imperial County) of internodes, deformed leaves and thickened twigs. Belize (Belize City, September 1999 Heavy infestations may result in plant death. Infested Belmopan) Venezuela November 1999 flowers often drop and usually there is little or no fruit (Margarita Island) production. Infested fruits are small and deformed, Barbados August 2000 resulting in reduced production and marketability. The Bahamas December 2000 insects also produce large quantities of Antigua February 2001 which encourages growth of black sooty molds on the Dominica June 2001 leaves. This results in reduced photosynthetic capacity. Biological control of Maconellicoccus hirsutus 243

HMB also produce white fluffy wax which covers most Table 2. An indicative list of important host plants of M. hirsutus stages as well as the ovisac. The wax is protective in in the Caribbean (Kairo 1997) function and is impermeable to water and most pesti- Type of plant Common name Scientific name cides. The presence of large quantities of wax reduces the aesthetic and commercial value of ornamentals. Ornamental Ornamental hibiscus Hibiscus rosa-sinensis Ginger lily Alpinia purpurea Forest trees Blue mahoe Hibiscus elatus Pest status and host range Samaan Tectona grandis Hog plum Spondias mombin In Egypt, Albizia lebbek (Leguminosae), mul- Fruit trees/ Soursop muricata berry (Morus alba: Moraceae) and Hibiscus spp. other crops Sugar apple Annona squamosa (Malvaceae) were most severely affected (Bartlett Red plum Spondias purpurea 1978). In India, HMB was initially a serious pest of Yellow plum S. purpurea var lutea Carambola Averrhoa carambola fibre crops such as jute (Corchorus spp.: Tiliaceae), Barbados cherry Malpighia glabra mesta (Hibiscus cannabinus) and roselle (Hibiscus Sapodilla Manilkara zapota sabdariffa). Later, it became a major pest of grapevines Ochro Abelmoschus (Vitis vinifera: Vitaceae) requiring regular intervention. esculentum Globally, HMB has been reported on more than 200 Hibiscus sabdariffa Cotton Gossypium hirsutum plant species (Stibick 1997). At the height of HMB Cocoa Theobroma cacao outbreaks in the Caribbean, over 170 plant species Citrus spp. were attacked in Grenada, Trinidad and Tobago and Weeds Man-better-man Achryanthes indica St. Kitts. These included fruit and forest trees, orna- Broomweed Sida spp. mental shrubs, annual crops and weeds (McComie 1997). The list of affected species included all plants losses at EC$ 9.7 million (US$ 3.6 million) and annual on which the mealybug was found and/or showed losses at EC$ 9.3 million (US$ 3.5 million) but with damage symptoms. Kairo (1997) suggested that when the recognition that losses to the Grenadian economy in large numbers of crawlers produced on suitable hosts general were expected to be substantially higher. How- such as samaan (Samamea saman) were dispersed by ever, these estimates did not include costs associated wind, these settled indiscriminately on a wide range of with loss of trade or control of the pest. More recent plants. Many of these were incidental hosts on which data which include these elements estimate losses in crawlers were able to establish and produce symptoms, Grenada for the period 1995–1998 at US$ 18.3 million but which were not suitable for supporting mealybug (Peters 1999). The costs of the control programme for development and reproduction. Such plants were still the period were estimated at EC$ 2.9 million (US$ 1.1 recorded as hosts although it has now been shown that million). In St. Kitts, Francis (1999) estimated that for HMB is not economically important in many vegetable the period October 1995 to January 1997, economic crops reported as host plants. Indeed, once pest popu- losses amounted to US$ 280,000 inclusive of control lations were brought under control by the introduction costs. Additionally, in 1997 onion production experi- of natural enemies, fewer than 20 plant species were enced a loss of over US$ 22,000 in exports to regional found to support significant infestations of the HMB markets. Potential losses to agriculture and forestry (Table 2). in Trinidad and Tobago were estimated at US$ 125 million (PMC 1996). However, in a recent study of Economic losses the socio-economic impact of the hibiscus mealybug in Trinidad (Singh 1999) it was indicated that costs HMB is perhaps one of the few Caribbean pests for of over US$ 5.1 million were incurred up to 1997. which a detailed analysis of economic loss has been At the same time, estimated net benefit for the period undertaken, at least in some of the affected countries. 1996–2024 was US$ 41 million. This represented a Different approaches were used in different countries socio-economic benefit/cost ratio of 8 : 1. Other reports to estimate the losses but generally they have included of the economic impact of this pest indicated some US$ an assessment of direct loss to production and in some 67,000 for St. Lucia (Anon. 1999a) and US$ 3.4 million cases losses due to trade restriction and cost of con- for St. Vincent and the Grenadines (Edwards 1999). trol. In Grenada, Francois (1996) estimated one-time 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 involved advisory missions to countries. These mis- invaded production areas. However, there was an uncal- sions were carried out jointly by scientists from CABI culated economic impact on the agricultural sector due Bioscience, FAO and CARDI. to loss of regional export markets (Anon. 1999b). In a In 1996, the United States Department of Agri- recent analysis, the potential losses in the USA were culture, and Plant Health Inspection Service estimated at US$ 750 million per year (Moffit 1999). (USDA-APHIS) in collaboration with the Ministry Agricultural crops in the mainland US expected to bear of Agriculture St. Kitts and Nevis, initiated a par- most of the economic risk were ornamentals, vegeta- allel program. CABI Bioscience provided an initial bles, citrus, cotton, grapes and . This interest- stock of A. kamali which was multiplied and released, ing analysis is based on the projected distribution of while stocks of C. montrouzieri were obtained from a HMB predicted by CLIMEX modeling. commercial insectary in the USA. Indeed, most other countries that implemented biological control subse- quently obtained stocks of C. montrouzieri from the Biological control same source. In addition USDA-APHIS initiated an exploratory programme through which another para- Biological control initiatives sitoid, Gyranusoidea indica Shafee, Alam and Agarwal (Hymenoptera: Encyrtidae) collected in Egypt, was The biological control effort was initiated in 1995 introduced. USDA-APHIS activities were subse- when the FAO funded a project for Grenada (TCP/ quently transferred to St. Thomas, US Virgin Islands GRN/4553). Through the project, CABI Bioscience and Puerto Rico, where these were focussed on control assisted with the introduction of A. kamali,an of the pest in US Territories in the Caribbean. USDA- encyrtid parasitoid of the mealybug from China. APHIS was also instrumental in the organization of When Trinidad became infested in 1996, CABI several technology transfer workshops and the produc- Bioscience also assisted with introduction of the tion of a training manual (Meyerdirk et al. 1998). parasitoid in a project funded by the Trinidad CARINET, the Caribbean LOOP of BioNet Interna- and Tobago Government. At the same time, the tional in collaboration with CABI Bioscience and other Caribbean Agricultural Research and Development agencies was instrumental in organizing two regional Institute (CARDI) assisted with introduction of two training workshops in mealybug identification. This coccinellids, C. montrouzieri and coccivora resulted in the production of an identification man- Ramakrishna Ayyar (Coleoptera: Coccinellidae), from ual in English and Spanish (Watson & Chandler 1999, India. Faced with a rapidly spreading problem, gov- 2000). The Inter-American Institute for Cooperation in ernments in the region requested assistance from FAO Agriculture (IICA) also assisted capacity building and to deal with the situation. In 1996, a regional project in collaboration with CARDI addressed post harvest was approved. Initially, the beneficiary countries of the issues (Gautam et al. 2000; IICA 1999). project included all 13 independent Caribbean Com- A vital component of the biological control efforts munity (CARICOM) member countries (Antigua and was the part played by national institutions. Most of Barbuda, Bahamas, Barbados, Belize, Commonwealth the countries established national taskforces to specifi- of Dominica, Grenada, Guyana, Jamaica, St. Kitts and cally deal with the problem. In affected countries, these Nevis, Saint Lucia, St. Vincent and the Grenadines, taskforces dealt with the tactical issues with regard to Suriname, Trinidad and Tobago) and Venezuela. Sub- control. In threatened countries, they played a more sequently, Cuba was also included as a beneficiary strategic role both in planning detection programs and country. The overall objective of the project was to eventual control. In some cases they were also respon- support regional activities towards a long-term sus- sible for dealing with matters relating to trade. tainable control of the HMB in the Caribbean Sub- Region. There were three broad areas of activity under Natural enemies of HMB and use in the project – the actual biological control programme, a biological control public awareness component and training. CABI Bio- science was responsible for the biological control com- The natural enemy complex of HMB in India and Egypt ponent, while CARDI was responsible for the public is well known (Kamal 1951; Ghose 1970; Beardsley awareness. The training component was undertaken as 1985; Mani 1989). This includes at least 30 species, a joint activity. An important component of the project 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 USDA-APHIS A. dactylopii China CABI Bioscience

Neuroptera, Lepidoptera, Diptera and Coleoptera. The in Grenada and subsequently to most of the affected parasitoid complex comprises at least 16 species countries. of parasitoids in six Hymenopteran families. The A. kamali is a solitary endo-parasitoid. Like many most important species belong to the encyrtid genus encyrtids, adults also host feed and this may contribute Anagyrus, notably A. kamali, A. dactylopii (Howard), considerably to the overall mortality (Noyes & Hayat A. aegyptiacus Moursi and an unidentified species. 1994). Moursi (1948) gives the earliest account on its Another encyrtid, Leptomastix phenacocci Compere, biology. Kairo et al. (1997) provide some details of its has also been reported as important. More recently, development, particularly in relation to rearing. More G. indica was collected in Egypt, Pakistan and Aus- recent studies have concentrated on host stage pref- tralia (USDA 1999). Among the predators, coccinellid erence, host immune response and life table statistics are the most important. Species of particular (Sagarra et al. 2000; Sagarra & Vincent 1999; Persad & note include C. montrouzieri, S. coccivora, Scymnus Khan (in press)). sp. nr. nubilis Mulsant, S. conformis Jordan and Bru- G. indica was collected by USDA-APHIS in Egypt, moides suturalis (F.). The natural enemy species that Pakistan and Australia and introduced initially to have been introduced into the Caribbean or considered St. Kitts. It has also now also been released in USVI, for introduction are listed in Table 3 and these are dis- Puerto Rico, Grenada, Belize and California. The par- cussed below. asitoid reportedly became established in St. Kitts and other locations, based on data from impact assessment studies at several release sites (Meyerdirk 1999). There Parasitoids is little information available on its biology beyond the Two parasitoids have been introduced and released fact that it is a solitary endo-parasitoid. against HMB and these are A. kamali and G. indica. A third parasitoid, A. dactylopii, was also considered Predators but was not introduced. A. kamali was the first natural Two predators were introduced for control of HMB, enemy to be introduced into the Caribbean for con- C. montrouzieri and S. coccivora. Because of its wide trol of HMB. The recommendations to introduce this host range, C. montrouzieri has been used for con- parasitoid were based on previous successful introduc- trol of many other mealybug species including control tion against HMB in Egypt (Kamal 1951). This was of HMB in Egypt and India (Bartlett 1978; Moore supported by the fact that the fortuitous introduction 1988). In Egypt, large numbers of C. montrouzieri of A. kamali and another Anagyrus sp. was appar- were released from 1922 but although it become estab- ently one of the reasons why HMB was not serious in lished it was not effective because of poor survival dur- Hawaii (Beardsley 1985). In India, Anagyrus spp. were ing winter (Hall 1926). In India inoculative releases also reported as important natural enemies of HMB of C. montrouzieri to control HMB on grapes have (Ghose 1971; Mani 1989). Finally, available informa- been quite successful (Mani 1988). On this basis, tion showed that this parasitoid had a narrow host range C. montrouzieri was selected for introduction. An area (Cross & Noyes 1995). The parasitoid was first released 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 Implementation of the Code of Conduct for pressure to control HMB rapidly negated serious con- the Import and Release of Exotic sideration of such concerns in many countries, at Biological Control Agents least initially. In the Caribbean, C. montrouzieri has been released widely and was particularly significant Recent years have seen increased concerns over the in rapidly bringing down high populations. However, potential impact of introduced agents on non-target as a high density feeder, its ability to maintain low species (Howarth 1991; Simberloff & Stiling 1996; pest populations was considered to be limited. Indeed Thomas & Willis 1998). In 1996, the ‘Code of Conduct there were concerns that the predator would become for the Import and Release of Exotic Biological Con- extinct. It is noteworthy that although the predator was trol Agents’ was ratified by FAO member countries previously introduced into several Caribbean islands under the International Plant Protection Convention where it became established, for instance, in St. Kitts (FAO 1996). The Code provides guidelines to be fol- (Cock 1985), it was apparently absent when HMB lowed when making introductions of natural enemies, was introduced. While there is potential for the preda- outlining the responsibilities of both exporting and tor to be used against many mealybug species, its importing agencies. One of the requirements of the use in the future may be limited because of con- Code is the production of a dossier containing infor- cerns about the potential negative impact on non-target mation on the host range, as well as risks associated organisms. with introduction of any particular natural enemy. The C. montrouzieri has been widely studied. Accounts purpose of the dossier is to enable importing coun- of the developmental and reproductive biology are tries to make an informed judgement on whether or given by Bhat et al. (1983), Satyanarayanamurthy and not to introduce a natural enemy. Dossiers were pre- Lakshmi Narayana (1986), Balakrishnan et al. (1987), pared on all the natural enemies introduced under the Mani and Thontadaraya (1987), Mani (1988), Gau- FAO funded projects. A dossier on A. kamali was first tam (1996) and Kaufmann (1996). Mechanisms of host prepared by Cross and Noyes (1995) and this was sub- location have been studied by Heidari and Copland sequently revised by Kairo and Peterkin (1998). Sim- (1992 1993) and Merlin et al. (1996a,b). Both lar- ilarly, dossiers on C. montrouzieri and S. coccivora vae and adults of C. montrouzieri feed on the hosts were first prepared by Gautam and Parasram (1996a,b). and detailed studies on consumption rates are reported These were revised extensively by Peterkin et al. by Babu and Azam (1988), Mani (1988), Mani and (1998a,b) following additional studies and also to con- Thontadarya (1987), Oncuer and Bayhan (1982) and form more specifically to the Code. USDA-APHIS Reddy et al. (1991). prepared an Environmental Assessment (EA) prior to Unlike C. montrouzieri, S. coccivora has no previ- introduction of A. kamali and G. indica in St. Kitts ous history of successful introduction. The predator (Meyerdirk 1997). This EA was prepared following US was introduced into the USA from India in 1956 but regulations on import and release of exotic natural ene- followup data are not available (Gordon 1985). The mies and served a similar purpose as the dossiers. species was also introduced from India to the Bahamas During the implementation of the work programme, for control of Pulvinaria maxima Green in 1956–57 but it was clear that most national programs did not have did not become established (Cock 1985). S. coccivora specific mechanisms in place to regulate the introduc- has been released in several countries in the Caribbean tion of natural enemies. It is clear that there is an urgent for control of HMB including Trinidad and Tobago, need for this to be addressed. Much still has to be done St. Kitts, British Virgin Islands and Grenada. Initial to develop the framework for implementation of the indications suggested that it had become established Code. There is a need to develop the necessary legal in some of the countries. However, subsequent stud- framework and identify responsible authorities within ies in Trinidad, where the most releases were made, countries. It is essential for biological control practi- suggest that it is rare (Ramroop & Peterkin 1999). Its tioners to foster implementation of the Code. contribution to HMB control has been minimal if at all. Accounts of the developmental and reproductive Natural enemy introductions into countries biology of S. coccivora are given by Gautam (1996), Mani and Thontadarya (1987), Padmaja et al. (1995) Introduction and rearing natural enemies and Peterkin et al. (1998b). 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 Table 4 gives a list of natural enemies introduced from China through collaboration with the Guangdong into different countries. A. kamali and C. montrouzieri Entomological Institute. Subsequently, USDA-APHIS have been introduced into all the countries where the procured A. kamali from Hawaii. C. montrouzieri and pest is present. The other two natural enemies have S. coccivora were initially sourced from India through been introduced into only some of the countries. a collaborative programme between the Indian Agri- cultural Research Institute (IARI), CARDI and the Release strategies Ministry of Agriculture Land and Marine Resources, In most cases, the species and numbers of natural ene- Trinidad and Tobago. Subsequent introductions were mies released were dictated by availability. The choice made from commercial suppliers in USA and UK. of release sites was based on location where infesta- G. indica was procured from Egypt through the USDA- tions occurred first. For instance, in most countries, APHIS programme. After the initial introductions, initial infestations of HMB were usually in urban areas natural enemies were supplied to countries by several where mainly ornamentals and fruit trees were affected. agencies and national programs as listed below: The distribution of such plants was often discontinu- ous but this does not appear to have posed a problem (a) CABI Bioscience facilities in the UK and Trinidad with the establishment of natural enemies. It is possi- (A. kamali and S. coccivora). ble that because of the wide host range of HMB, what (b) USDA-APHIS facilities in Newark and St. Thomas appeared as a discontinuous distribution was perhaps (A. kamali and G. indica). fairly continuous allowing natural enemies to move (c) National programs particularly in St. Kitts (in col- between affected plants. laboration with USDA-APHIS) and Trinidad and Because of the distribution of affected plants in small Tobago (A. kamali, G. indica, C. montrouzieri and clumps, numbers of natural enemies released at each S. coccivora). site varied and was based on simple practical consid- (d) Commercial suppliers in the US and UK specifi- erations. For C. montrouzieri, releases comprised of a cally for C. montrouzieri. few individuals per bush to several hundred in case of Due to the lack of adequate facilities for rearing large trees. In the case of A. kamali, releases varied natural enemies, many of the countries had to rely from about 50 per bush to several hundred per hedge entirely on supply of natural enemies from outside in the case of hibiscus or for large trees. Releases at sources. Quarantine of natural enemies within target each site were usually in hundreds (Kairo et al. 1999). countries was not possible but specific measures were However, it is important to note that overall the major taken to ensure that only clean material was intro- determinants of numbers released were availability and duced. Under the CABI Bioscience programme, the size of pest population. measures included a system of rigorous checks at each An important consideration was whether to sepa- stage of the rearing process to ensure that cultures were rate the releases of C. montrouzieri and A. kamali clean. Additionally, only adult insects were shipped both spatially and temporally. Apart from direct com- thus allowing a final check to verify species identity. petition for hosts, there was also the possibility that The specific measures taken for each natural enemy C. montrouzieri would feed on parasitized mealybugs, are detailed in the dossiers. Thus, it was possible for thus reducing the chances of establishment of the intro- countries to review the procedures in advance to satisfy duced parasitoids. Therefore, where possible, efforts themselves that the shipments met their requirements. were made to separate releases. In view of the sug- It is assumed that other programmes supplying nat- gestion that C. montrouzieri is a high density feeder, ural enemies followed similar procedures. Exchange the predator was released first followed by A. kamali a of natural enemies between national programs was few weeks later. However, while no studies were con- possible following establishment of rearing facilities ducted to assess the effectiveness of this strategy, the in some of the countries. The techniques for rearing success of the approach, where implemented, indicates natural enemies varied from complex systems, partic- its practical value. ularly for the parasitoids, to simple systems involv- An interesting component of the release programme ing use of field collected host material as food, e.g. was the involvement of the public, particularly in for C. montrouzieri. Several laboratory rearing manu- redistribution of C. montrouzieri (Stewart 1999). This als were developed (Gautam 1996; Kairo et al. 1997; proved very effective in Trinidad and Tobago, and was Meyerdirk et al. 1998). 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 ? ?

1Denotes 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 release period is debatable, as countries which made on the availability of natural enemies and concerns releases over specific time periods such as St. Lucia over apparent upsurges of the pest, particularly in and St. Kitts achieved similar levels of control. the dry season. Thus in cases where countries had the capability to rear natural enemies, releases were Prophylactic releases continued over several years, particularly in Grenada, The possibility of making ‘prophylactic releases’, that and Trinidad and Tobago. The value of the extended is the pre-emptive release of natural enemies as a Biological control of Maconellicoccus hirsutus 249 preventative measure, was considered in some of the have shown a distinct and significant role of A. kamali affected countries. For obvious reasons the strategy in controlling HMB (Meyerdirk 1999). was only possible for a generalist natural enemy such Detailed studies were carried out to quantify popu- as C. montrouzieri which could survive on other hosts. lation growth parameters of A. kamali, C. montrouzieri Towards this end, the predator was released in Barbados and S. coccivora under laboratory conditions (Persad and Dominica. While Dominica and Barbados have 1999). Under field conditions, C. montrouzieri was only recently become affected, this cannot be attributed very effective in reducing HMB populations and this to the prophylactic releases. It should be noted that was demonstrated by McComie et al. (1999). Stud- the chances of even such a generalist natural enemy ies carried out by Meyerdirk (1997) in the northern becoming established are small since most potential Caribbean, appear to support the notion that A. kamali hosts are likely to be rare, being themselves under is particularly important in maintaining low densities good natural control. Indeed anecdotal evidence from of the pest. At the outset, there was doubt as to whether Barbados suggests that the released material may have C. montrouzieri, a high density predator, would persist died out (Lennox Chandler, personal communication). when HMB populations became low. There is evidence Therefore, as yet, there is no evidence to the authors’ which shows that it has in actual fact continued to per- knowledge where such releases have been effective. In sist in the field two years after introduction in some view of the concerns over possible impact on non-target of the countries. Whether or not it will persist in the organisms by generalist natural enemies, it is unlikely long term remains to be seen. No studies have been that such a strategy will be of practical value in future carried out under field conditions to compare the rela- biological control programmes. tive contribution of each of the introduced natural ene- mies. However, there is some evidence suggesting that A. kamali may displace G. indica under field conditions Establishment and impact of natural enemies (Meyerdirk, personal communication). A. kamali, C. montrouzieri and G. indica became established in all countries where they were released (Table 3). However, although recovered a few months The current status after release, there is little evidence to show that S. coccivora became established, even in Trinidad A regional workshop was organized at the conclusion where most of releases were made. Interestingly, of the FAO project in March 1999 to assess the progress A. kamali and G. indica appear to have become for- with the biological control programme (Anon. 1999c). tuitously introduced into at least two islands, Curac¸ao It is quite clear that in all the countries where biological and Trinidad, respectively. The appearance of G. indica control has been implemented, this has resulted in very in Trinidad in 1999 was intriguing, as the majority of good control. However concerns about the effective- releases of the parasitoid had been made in the northern ness of control on certain crops have been expressed Caribbean. It would seem to suggest that mealybug (Peters 1999). The most notable are soursop (Annona infested material was still getting into Trinidad (Anon. muricata) and sorrel (Hibiscus sabdarifa). Populations 2000). Of particular note was the difficulty in getting of the pest apparently build up to high levels before establishment of both A. kamali and C. montrouzieri natural enemies can bring them under control. There on blue mahoe in the Grand Etang area in Grenada. is a need for detailed studies to understand the pop- Despite repeated releases of these natural enemies in ulation dynamics of the pest and natural enemies on this area, recoveries were always very poor. Inter- these crops, in order to determine how serious the estingly, populations of HMB on this tree appear to problem is and to identify windows of opportunity for have diminished anyway, possibly due to plant related intervention. factors. The type of studies carried out to assess impact of Factors leading to rapid success with biological natural enemies varied considerably from country to control of HMB in the Caribbean country. Countrywide surveys were conducted in sev- eral countries notably Grenada, Trinidad and Tobago, Because natural enemies of HMB were already known, St. Vincent and the Grenadines, and Guyana but the it was possible to make arrangements for their sup- results have not been published. In the US territories, ply to the Caribbean within a short space of time. For and St. Kitts and Nevis, population counts were made instance, CABI Bioscience linked with collaborators at specific sites mainly by sampling hibiscus. These 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 most countries, this was purely an academic question. able to obtain initial stocks of C. montrouzieri and Results of control were seen in renewed production of S. coccivora for subsequent release and rearing. How- those crops that had been particularly badly affected ever, once an inexpensive source of C. montrouzieri such as (Annona spp.), plums (Spondias was identified from commercial sources in the United spp.), sorrel (Hibiscus sabdariffa), (Abelmoschus States of America, the predator was subsequently pro- esculentus) etc. Ornamental hibiscus is once again cured by many national programs from this source. flourishing, whereas there was a time when flower- Through the regional FAO funded project all coun- ing hibiscus shrubs were rare. More importantly, trade tries, including non-beneficiary ones, were supplied between infested and uninfested countries has been with natural enemies, particularly A. kamali, when resumed to some extent, following the development of requested. There was tremendous goodwill and collab- export protocols. oration between national programs, regional and inter- Severe devastation of natural habitats as seen, for national organizations towards the biological control example, in the Grand Etang area in Grenada where effort. a stand of 38 ha of blue mahoe (Hibiscus elatus) Because many ornamental plants, home gardens and was destroyed, has now been averted elsewhere. For field crops were affected, the wider population had a small island states, such severe damage has poten- great interest in the control of HMB. Effective pub- tially serious long-term effects. Furthermore, there lic awareness programmes ensured cooperation. Thus is no doubt that continued application of chemical adverse measures such as indiscriminate spraying with pesticides would have been harmful to humans and chemical pesticides or removal of plants which could the environment. have negatively affected the biological control effort Many of the affected countries in the Caribbean were avoided. In Trinidad and Tobago, and other coun- were ill-prepared to mount a classical biological control tries, the public also played a key role in redistri- project. With few exceptions there was a general lack bution of the biological control agents, particularly of trained personnel and insect rearing facilities. How- C. montrouzieri. ever several countries established rearing facilities, for Following the extensive devastation in Grenada, instance, Grenada, Guyana, St. Kitts and Nevis, and regional governments recognized the danger posed by Trinidad and Tobago. Similarly several training courses the pest and allocated resources towards the man- were held and staff were attached to laboratories rear- agement of the pest. The response of international ing natural enemies. Suffice to say that there is now a organizations/funding agencies, most notably FAO, in cadre of trained personnel in most countries, able to supporting a regional biological control effort was cru- implement a biological control programme. cial to the success achieved. Clearly, the need for a rapid One of the important benefits of the project is that reaction capability such as that provided by the FAO it established in the minds of many stakeholders – Technical Cooperation Programme is vital to facilitate farmers, policy makers and politicians, householders quick action to deal with new invasive pests that can be etc. – that biological control is a viable alternative to targeted for biological control. chemical pest control and a practical solution to some pest problems. This has provided good publicity for Benefits from the programme biological control which can only make it easier to pro- mote as a component of IPM programmes. Apart from economic benefits, the programme also contributed to safeguarding both environmental and Quarantine, pest detection and identification human health. It also resulted in development of capac- ity to undertake biological control programmes. More The importance of quarantine in preventing the intro- importantly, it has set the scene for implementation of duction of exotic pests can not be over-emphasized. integrated pest management. These benefits are dis- The first step in dealing with any invasive pest is cussed in greater detail below. timely detection and correct identification. The ini- The economic benefits derived from successful con- tial invasion of HMB in Grenada probably went unde- trol of HMB were enormous. One only needs to con- tected for two years. The reasons for this are not clear sider the estimated losses (above) to appreciate this. but by the time the pest was identified, it had spread While there is a limited amount of detailed eco- throughout Grenada. Experiences in other countries logical data on the impact of natural enemies, for that became affected subsequently, showed that early Biological control of Maconellicoccus hirsutus 251 implementation of biological control slowed spread of and release of exotic natural enemies, a significant step the pest and substantially curtailed damage. Thus, it forward in the implementation of pest con- is vital for countries to institute mechanisms to allow trol. The programme for control of HMB has served to early detection of exotic pests. While correct identifica- develop capacity in biological control and taxonomic tions were made in the case of HMB, it is important to skills within Caribbean national systems and also to note that the literature has several spectacular examples popularize biological control in the widest sense. where incorrect identification of the pests hindered and Scientifically, it is interesting in that both general- slowed implementation of biological control. Further- ist and specialist natural enemies were used. Although more, the presence of a pest may have serious implica- there is a limited amount of ecological information, it tions for trade. Greater emphasis will need to be placed is clear that A. kamali alone can control the pest but in future on the development of skilled personnel and this takes a longer period. Thus although the generalist in the allocation of necessary resources to ensure that predator, C. montrouzieri may give a rapid reduction effective quarantine measures are implemented. of pest populations, its introduction can be avoided if A. kamali is introduced early. However, there is a Future opportunities dearth of empirical data on ecological assessment of the impact of these natural enemies. Particular areas of Mealybugs and indeed other Homoptera are easily interest would be the relative contribution of each of transported on plant material and the danger of new the natural enemies to the control achieved. The appar- introductions is ever present. Clearly, not all introduced ent persistence of C. montrouzieri is worthy of further species have become serious pests and there are many study as well as the impact of these natural enemies on possible reasons for this. For instance, some of the non-target organisms. Because of the possibility of con- species may have been introduced with their natural ducting comparative studies on the different islands, the enemies. There are several examples of this happen- Caribbean would be ideal for carrying out such stud- ing but perhaps most relevant is the case of HMB in ies. Further research is also needed to develop ways Hawaii (Beardsley 1985), and in Trinidad and Curac¸ao of enhancing the effectiveness of natural enemies in (cited above). It is also possible that indigenous nat- some cropping systems notably on soursop and to a ural enemies may adapt to effectively suppress popu- lesser extend on sorrel. lations of the invading species. It would be expected that that mealybug species with restricted host range Acknowledgements are less likely to become apparent when introduced, particularly if their hosts are not widespread or of eco- We wish to thank, several persons for sharing nomic importance. 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