hirsutus (pink ) Management and Control September 2010

Contents 1.0 Introduction……………………………………………………………Page 1 2.0 Monitoring……………………………………………...…...…………Page 1 3.0 Preventative Measures...………………………………………………Page 2 4.0 Chemical Control……………………………………………………...Page 4 5.0 Physical Control……………………………………………………….Page 4 6.0 Biological Control……………………………………………….…… Page 4 7.0 Integrated Management……………………………….………………Page 6 8.0 References………………………………………………………………Page 6

1. Introduction is a polyphagous pest which feeds on a wide range of important species including but not restricted to; , guava, , grape, , rose, , coconuts, , sugar cane, soursop, , cotton, and other fiber crops (Ranjan, 2006; Ujjan & Shahzad, 2007; Reddy et al., 2009). The feeding of M. hirsutus causes malformation of shoots and leaves believed to be caused by the injection of a toxic saliva (Kairo et al., 2000). In addition to lowering the aesthetics of the plant, this deformation can also result in lowered crop yields and in heavy infestations, plant mortality (Kairo et al., 2000; Chong et al. 2008). Like other sap sucking , M. hirsutus also excretes a sugary honeydew on which sooty mold develops, further deteriorating the quality of the agricultural or forest product (Gonzalez-Gaona et al., 2010). The presence of large quantities of wax, characteristic of M. hirsutus infestations, also reduces the aesthetic and commercial value of ornamentals (Kairo et al., 2000). The overall annual cost of control and damages to the US economy from M. hirsutus is estimated to be around US$ 700 million, with the global estimate being around US$ 5 billion (Ranjan, 2006).

2. Monitoring Previously, the monitoring methods for Maconellicoccus hirsutus in new locations involved visual inspections and the analysis of samples from potential host plants, followed by the taxonomic determination of collected individuals (Gonzalez- Gaona et al., 2010). However, this process only can be used to detect infestations which are already present (Gonzalez-Gaona et al., 2010). Furthermore, Vitullo et al. (2009) looked at feeding symptoms of different Hibiscus cultivars and found that not all cultivars exhibit signs indicating the presence of M. hirsutus, implying that feeding symptoms are not a reliable indicator of infestation.

Another method described by Serrano et al. (2001; Gonzalez-Gaona et al., 2010) involves the use of captive virgin female individuals in a trap as an attractant for male individuals. This method is impractical because of the difficulty of obtaining this type of female, their short life span, the risk of accidentally increasing pest populations and because it is not applicable in pest free areas bordering on the infested zones (Gonzalez-Gaona et al., 2010).

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Gonzalez-Gaona et al. (2010) demonstrated that a female sex pheromone developed by Zhang et al. (2004; in Gonzalez-Gaona et al., 2010) and composed of a mixture of lavandulyl and maconellyl in a 1:5 ratio significantly attracted males of M. hirsutus into traps and was also very specific. With the use of this pheromone in traps it was also possible to map the distribution of this species on a regional scale (Gonzalez-Gaona et al., 2010). In their experiment within plantations, red delta Biolure® traps containing a sticky substance on the interior base were installed with at least 20 m between them. 1 µg of the pheromone was placed in a grey rubber septum and placed inside the traps which were hung from the trees at a height of 1.5 to 3.0 m. For regional geographic distribution mapping, the traps were hung from trees at the edges of the highways and were between 4 and 6 km away from each other (Gonzalez-Gaona et al., 2010). Delta traps created from Tetrapack® waxed cardboard (from milk cartons) with an adhesive (such as Stickem®) applied to the bottom edge can also be utilised effectively with the pheromone placed inside (Gonzalez-Gaona et al., 2010).

The effectiveness of three commercially available traps were compared by Francis et al., (2007) and Vitullo et al., (2007). Francis et al., (2007) found that Delta traps and double sided sticky cards caught more adult males than Jackson traps, while the Delta and Jackson traps were more effective at minimizing the capture of non- target insects. Conversely, Vitullo et al., (2007) found that Jackson traps caught as many or more males per square centimeter of trapping surface as those with larger surfaces (including the Delta traps), and the time required to count males in Jackson traps was significantly less than in green Delta, Pherocon IIB, and Pherocon V traps (Vitullo et al.,2007). Jackson traps also had the advantage of requiring only the sticky liners to be replaced as opposed to the other traps which must be replaced entirely or inspected in the field and then redeployed (Vitullo et al., 2007). These differing results perhaps could be attributed to the different timings and localities of the field trials with both taking place in Florida but with Francis et al., (2007) conducting theirs in April / May, 2005 in horticulture research plots while Vitullo et al., (2007) conducted theirs in September / October, 2005 in residential areas, parks and golf courses in addition to horticulture research plots. Fewer males were caught in the traps as the age of the lure increased, with significantly fewer caught in traps that had been pre-aged for 2 months (Francis et al., 2007).

3. Preventative Measures Following the introduction of M. hirsutus from Grenada to Trinidad in 1994, quarantine systems were strengthened and upgraded in all the neighbouring countries to prevent or delay introduction (Sagarra & Peterkin, 1999). Legislation was enacted in several countries. For example, in Trinidad and Tobago, M. hirsutus was proclaimed to be a "Notifiable Pest" in October 1995. This was followed by the revision of the plant protection regulations and the increased surveillance at ports of entry. Regional plant protection officers were trained in Trinidad to identify mealybug species and a regional public awareness campaign for the West Indies was conducted to increase public knowledge and to consequently decrease illegal trading and contraband by exporters, importers and passengers (Sagarra & Peterkin, 1999). The impact of these measures was limited, as M. hirsutus went on to spread to over 25 islands between 1994 and 2001 (Kairo et al., 2000).

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The prophylactic or pre-emptive release of the generalist biological control agent Cryptolaemus montrouzieri was used on Barbados and Dominica in an attempt to prevent the spread of M. hirsutus (Kairo et al., 2000). However there has been no evidence that such releases have been successful, with M. hirsutus eventually invading both islands (Kairo et al., 2000).

Two hour laboratory fumigation of M. hirsutus using 48 mg/liter of methyl bromide was found to result in 100 % mortality of all life stages and has been suggested to provide quarantine security for infested commodities for export or import (Zettler et al., 2002). Methyl bromide, though, may adversely affect the quality of the treated crop and as a result should be used selectively on certain crops (Ranjan, 2006). It is also an ozone-depleting substance planned to be phased out by the Montreal Protocol (United Nations Environment Programme, 1992; in Follett, 2004) and as demand for it has subsequently gone down, prices have risen, creating a need for alternative methods of quarantine security (Follett, 2004).

The irradiation of M. hirsutus for the phytosanitation of agricultural commodities was investigated by Jacobsen & Hara (2003). Tolerance of M. hirsutus to irradiation was observed to increase with maturity with eggs, crawlers and nymphs sufficiently controlled by doses of 100 Gy and over but with adults still capable of producing viable progeny at 100 Gy (Jacobsen & Hara, 2003). At 250 Gy, complete sterility was achieved in 13824 eggs oviposited by 3093 adults (Jacobsen & Hara, 2003). It is therefore suggested by Jacobson & Hara (2003) that the minimum effective dose for quarantine security is between 100 and 250 Gy.

Follett (2004) investigated the use of heat vapour treatments to kill populations of M. hirsutus on agricultural commodities. On Chinese pea (Pisum sativum), treatments at 47 ºC required 45 min to kill all life stages whereas treatment at 49 ºC required only 10 min to kill all life stages with adults and nymphs being most tolerant to treatment at 47 ºC and the eggs being the most tolerant at 49 ºC (Follett, 2004). It is important to note that heat vapour treatment temperatures and times may vary across different hosts and that depending on the host, M. hirsutus may be able to remain protected and hidden, for example underneath the calyx in fruits like lime and persimmon (Follett, 2004).

The susceptibility of different M. hirsutus life stages when immersed into hot water was studied by Hara & Jacobsen (2005) for the development of a postharvest disinfestation treatment. Different life stages were immersed in water at 47, 48, and 49 ºC in 2 minute and 4 minute increments. The results suggest that all life stages of M. hirsutus should be controlled by the 20-min 49 ºC hot water immersion treatment approved for control of fruit flies in longan and lychee, with the immature crawler stage being most susceptible and the egg stage being the most tolerant to hot water immersion (Hara & Jacobsen, 2005).

4. Chemical Control

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In , granular insecticides have been shown to be ineffective while systemic insecticides are only used in heavy infestations (Mani, 1989; in EPPO, 2005). Additionally, inorganic oil emulsion sprays gave good control of M. hirsutus on guava (EPPO, 2005).

However, in general, the use of pesticides is ineffective against M. hirsutus, partly because of its habit of hiding in crevices (EPPO, 2005) and because pesticides cannot penetrate the heavy layers of wax that shield the body (Kairo et al., 2000). The egg stage in particular, is protected by a white, waxy ovisac, which most pesticides cannot penetrate (McKenzie, 1967; in Reddy et al., 2009). A number of different pesticides have been trialed for the control of M. hirsutus. However, even if a quick knockdown was achieved, rapid recolonisation made it necessary to repeat spray cycles every 2 – 3 weeks (Sagarra & Peterkin, 1999). This combined with the extremely wide host range and large host size of M. hirsutus makes it almost impossible to have a spraying program capable of bearing the cost and coping with the practicalities of treating the whole range of infested plants in an affected area (Sagarra & Peterkin, 1999).

Srinivas et al. (2007) compared four neem-based products for use as an alternative to potentially dangerous insecticides used in India such as dichlorvos. It was found that neem kernel extract and a commercially produced neem extract based product (Rakshak) induced mild ovicidal action and appreciable nymphal and adult mortality of M. hirsutus, comparable to the effect of dichlorvos (Srinivas et al., 2007).

5. Physical Control The pruning and burning of infested material has been used in an attempt to control M. hirsutus in places such as Trinidad following the discovery of infestation (McComie, 1996). However, these efforts are ineffective in slowing the spread of M. hirsutus (Sagarra & Peterkin, 1999).

The movement of infested plants and plant material is strongly not advisable as this may spread M. hirsutus to new areas (Bogran & Ludwig, 2007).

6. Biological Control Biological control is regarded as the most effective way to control M. hirsutus populations (Kairo et al., 2000; EPPO, 2005). A number of biological control agents have been trialled in different locations around the world with different levels of effectiveness.

Encyrtid wasps (Hymenoptera: Encyrtidae) have been used frequently as highly specific parisitoids of M. hirsutus (Kairo et al., 2000). These parasitoid wasps lay eggs within the adult individuals of M. hirsutus and include Anagyrus kamali from China, Allotropa sp. near mecrida from southern Egypt, Gyranusoidea indica from India and Leptomastix dactylopii from South America. The most well documented of these is A. kamali which was first released in Egypt in the 1930’s to great success with figures of parasitisation from field samples ranging from 66- 98% with reports that M. hirsutus was almost eradicated in some areas (Kamal, 1951; in Sagarra & Peterkin, 1999). Since then, the use of A. kamali has been successful on the majority of infested islands as well as Mexico and California (Kario

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et al., 2000; Roltsch et al., 2006; Garcia-Valente et al., 2009). While G. indica was also used on many Caribbean islands with great success, there is evidence that G. indica may be displaced by A. kamali under field conditions (Meyerdirk pers. comm.; in Kairo et al., 2000). Although Roltsch et al., 2006 observed that A. kamali showed higher levels of parasitism than G. indica in California, activity of G. indica was elevated during fall and winter and may therefore be responsible for significantly contributing to M. hirsutus mortality during winter.

On the other hand the results from A. sp. near mecrida and L. dactylopii have been less successful, with A. sp. near mecrida failing to establish in California after numerous releases in 2003 and 2004 (Roltsch et al., 2006) and no field recoveries of L. dactylopii made since its release on Barbados (Gibbs & Taylor).

Coccinellid beetles (Coleoptera: Coccinellidae) such as C. montrouzieri and Scymnus coccivora are also used as generalist predators of such as M. hirsutus and often released simultaneously with A. kamali and G. indica (Kairo et al., 2000). These beetles have been tested in India with C. montrouzieri solely responsible for the decline of M. hirsutus on sapota (from 54 .2/ plant to 1.5/ plant in two months) in Bangalore (Mani & Krishnamoorthy, 2008) and S. coccivora shown to be capable of reducing M. hirsutus populations by 68 % in 56 days (Baskaran et al., 2007). While C. montrouzieri also was used successfully in the Caribbean, S. coccivora was not, failing to establish in all the locations it was released (Kairo et al., 2000). Furthermore, it is important to note that while C. montrouzieri managed to successfully establish in Egypt in the 1930’s its effectiveness was limited due to poor survivability during the Egyptian winter (Hall, 1926; in Kairo et al., 2000).

The regional biological control program which was initiated in the Caribbean following the introduction and rapid spread of M. hirsutus to over 20 islands in five years was seen as a tremendous success due to two biological control agents in particular; C. montrouzieri and A. kamali (Kairo et al., 2000). This has been attributed to their rapid rate of reproduction, and to a public awareness programme to reduce use of plant protection products which would have been detrimental to the survival of the biological control agents (Kairo et al., 2000). While A. kamali is capable of controlling M. hirsutus alone, control is achieved more slowly without the concurrent effects of C. montrouzieri (Kairo et al., 2000). However, if A. kamali is introduced early enough, Kairo et al. (2000) state that the need to introduce C. montrouzieri can be avoided altogether.

Detailed information on life cycles and the rearing and maintenance of populations of A. kamali, G. indica, and C. montrouzieri as biological control agents for M. hirsutus can be located in Francis & Francis (2001).

Non-insect biological control agents have also been demonstrated to be effective in controlling populations of M. hirsutus. A study by Ujjan & Shahzad (2007) showed that three different strains of the pathogenic fungus Metarhizium anisopliae var. acridum infected adults of M. hirsutus within two days with 90 % adult mortality achieved within 8 days and 100% of instar mortality achieved by the 4th day. However, while the use of M. anisopliae may show promise in laboratory studies, more studies are needed regarding its biology and application in the field (Ujjan &

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Shahzad, 2007), especially as different levels of humidity and temperature are known to limit fungal development on insects (Glare & Milner, 2001; in Ujjan & Shahzad, 2007).

7. Integrated Management Biological control has been very effective in some areas, especially if utilised early, keeping populations of M. hirsutus low enough to not cause any noticeable impacts (eg. in Puerto Rico (Michaud & Evans, 2000)). However, as biological control will never achieve pest eradication, it is often used as a component of integrated pest management programs involving physical and/or chemical methods as well. For example, in India the predator C. montrouzieri is used with insecticides (dichlorvos and chlorpyrifos) to achieve control of M. hirsutus on grapevine (Mani, 1989; in EPPO, 2005). It is important to ensure that insecticides used will not cause injury to any natural enemies present (EPPO, 2005).

8. References Bográn, C. E., & Ludwig, S. (2007). Pink hibiscus healybug a new pest in Texas. Retrieved April 19, 2010 from AgriLife website: http://repository.tamu.edu/bitstream/handle/1969.1/87496/pdf_2517.pdf?se quence=1 Chong, J.H., Roda, A.L., Mannion, C.M. (2008). Life history of the mealybug, Maconellicoccus hirsutus (: Pseudococcidae), at constant temperatures. Environmental Entomology, 37(2), 323-332. European and Mediterranean Plant Protection Organization (EPPO). (2005). Data sheets on quarantine pests Maconellicoccus hirsutus. Accessed April 19, 2010 from EPPO website: http://www.eppo.org/QUARANTINE/insects/Maconellicoccus_hirsutus/DS _Maconellicoccus_hirsutus.pdf Francis, A., Bloem, K.A., Roda, A.L., Lapointe, S.L., Zhang, A.,Onokpise, O. (2007). Development of trapping methods with a synthetic sex pheromone of the pink hibiscus mealybug, Maconellicoccus hirsutus (Hemiptera: Pseudococcidae). Florida Entomologist, 90(3), 440-446. Follett, P.A. (2004). Generic vapor heat treatments to control Maconellicoccus hirsutus (Homoptera: Pseudococcidae). Journal of Economic Entomology, 97(4), 1263-1268. Garcia-Valente, F., Ortega-Arenas, L.D., Gonzalez-Hernandez, H., Villanueva- Jimenez, J.A., Lopez-Collado, J., Gonzalez-Hernandez, A., Arredondo- Bernal, H.C. (2009). Natural and induced parasitism of Anagyrus kamali against pink hibiscus mealybug on shoots in Bahia de Banderas, Nayarit. Agrociencia, 43(7), 729-738. Gibbs, I.H., & Taylor, B. (undated). A Review of the Biological Control Program for the Pink Hibiscus Mealybug Maconellicoccus hirsutus (Green)(Homoptera: Pseudococcidae) in Barbados: Problems and Progress. Retrieved April 19, 2010 from Barbados Ministry of Agriculture website: http://www.agriculture.gov.bb/files/mealybug.pdf Gonzalez-Gaona, E., Sanchez-Martinez, G., Zhang, A., Lozano-Gutierrez, J., Carmona-Sosa, F. (2010). Validation of two pheromonal compounds for monitoring pink hibiscus mealybug in Mexico. Agrociencia, 44(1), 65-73.

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Hara, A.H., & Jacobsen, C.M. (2005). Hot water immersion for surface disinfestation of Maconellicoccus hirsutus (Homoptera : Pseudococcidae). Journal of Economic Entomology, 98(2), 284-288. Jacobsen, C.M., & Hara, A.H. (2003). Irradiation of Maconellicoccus hirsutus (Homoptera: Pseudococcidae) for phytosanitation of agricultural commodities. Journal of Economic Entomology, 96(4), 1334-1339. Kairo, M.T.K., Pollard, G.V., Peterkin, D.D., & Lopez, V.F. (2000). Biological control of the hibiscus mealybug, Maconellicoccus hirsutus Green (Hemiptera: Pseudococcidae) in the Caribbean. Integrated Pest Management Reviews, 5, 241–254. McComie, L.D. (1996). Status of the hibiscus (pink) mealybug Maconellicoccus hirsutus (Green) programme in Trinidad. AGRIS Report. Retrieved April 19, 2010 from AGRIS website: http://agris.fao.org/agris- search/search/display.do;jsessionid=B900486A78470E6CD74E0947A2551 C52?f=1998/v2404/TT1998001013.xml;TT1998001013 Michaud, J.P., & Evans, G.A. (2000). Current status of pink hibiscus mealybug in Puerto Rico including a key to parasitoid species. The Florida Entomologist, 83(1), 97-101. Ranjan, R. (2006). Economic impacts of the pink hibiscus mealybug in Florida and the United States. Stochastic Environmental Research and Risk Assessment, 20, 353-362. Reddy, G.V.P., Muniappan, R., Cruz, Z.T., Naz, F., Bamba, J.P., & Tenorio, J. (2009). Present status of Maconellicoccus hirsutus (Hemiptera: Pseudococcidae) in the Mariana Islands and its control by two fortuitously introduced natural enemies. Journal of Economic Entomology, 102(4), 1431-1439. Roltsch, W.J., Meyerdirk, D.E., Warkentin, R.; Andress, E.R., Carrera, K. (2006). Classical biological control of the pink hibiscus mealybug, Maconellicoccus hirsutus (Green), in southern California. Biological Control, 37(2), 155-166. Sagarra, L.A., & Peterkin, D.D. (1999). Invasion of the Carribean by the hibiscus mealybug, Maconellicoccus hirsutus Green [Homoptera : Pseudococcidae]. Phytoprotection, 80(2), 103-113. Srinivas, T., Prasad, K.S., Shekhar, M.A., & Manjunath, D. (2007). Evaluation on neem based formulations vis-a-vis Dichlorvos against Maconellicoccus hirsutus. Uttar Pradesh Journal of Zoology, 27(1), 13-20. Ujjan, A.A., Shahzad, S. (2007). Pathogenicity of Metarhizium anisopliae var acridum strains on pink hibiscus mealy bug (Maconellicoccus hirsutus) affecting cotton crop. Pakistan Journal of Botany, 39(3), 967-973. Vitullo, J.,Wang, S., Zhang, A., Mannion, C., Bergh, C.J. (2007). Comparison of sex pheromone traps for monitoring pink hibiscus mealybug (Hemiptera : Pseudococcidae). Journal of Economic Entomology, 100(2), 405-410. Vitullo, J., Zhang, A., Mannion, C., Bergh, C.J. (2009). Expression of feeding symptoms from pink hibiscus mealybug (Hemiptera: Pseudococcidae) by commercially important cultivars of hibiscus. Florida Entomologist, 92(2), 248-254. Zettler, J.L., Follett, P.A., & Gill, R.F. (2002). Susceptibility of Maconellicoccus hirsutus (Homoptera: Pseudococcidae) to methyl bromide. Journal of Economic Entomology, 95(6), 1169-1173.

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