Brunei in 1979, Thailand in 1987, the Maldives, and Vietnam in 1994 (Williams. 2004), and is here recorded from Cambodia for the first time. Pseudococcus.
NOTE New Records of Invasive Insects (Hemiptera: Sternorrhyncha) in Southeast Asia and West Africa1 R. Muniappan,2 B. M. Shepard,3 G. W. Watson,4 G. R. Carner,5 A. Rauf,6 D. Sartiami,6 P. Hidayat,6 J. V. K. Afun,7 G. Goergen,8 and A. K. M. Ziaur Rahman9
J. Agric. Urban Entomol. 26(4): 167–174 (October 2009)
ABSTRACT Several sap-sucking insects (Hemiptera: Sternorrhyncha) of neotropical origin have been accidentally introduced to Southeast Asia and West Africa in recent years, including the mealybugs Paracoccus marginatus Williams & Granara de Willink, Phenacoccus madeirensis Green, Phenacoccus manihoti Matile-Ferrero, Phenacoccus solenopsis Tinsley, Pseudococcus jackbeardsleyi Gimpel & Miller, and the whitefly Aleurodicus dugesii Cockerell (Aleyrodidae). This paper documents new distribution records of introduced mealybugs and some other sap-sucking hemipteran insects (Coccidae and Diaspididae) in these regions and discusses progress in the biological control of some of these pests. KEY WORDS Aleyrodidae, Coccidae, Diaspididae, Pseudococcidae, Aleurodicus dugesii, Paracoccus marginatus, Phenacoccus manihoti, Phenacoccus solenopsis, Pseudococcus jackbeardsleyi, invasive species
During recent visits to Southeast Asia by scientists from Virginia Polytechnic Institute and State University and Clemson University who were participating in a USAID-funded Integrated Pest Management Collaborative Research Support Program (IPM CRSP), heavy infestations of sap-sucking insects Hemiptera: Sternorrhyncha were sampled and subsequently identified. Samples from West Africa were collected by scientists from the International Institute for Tropical Agriculture in the Republic of Be´nin. Most of these pests are of neotropical origin and they have been accidentally introduced into these tropical regions in recent
1
Accepted for publication 11 April 2011. IPM CRSP, OIRED, Virginia Polytechnic Institute and State University, 526 Prices Fork Road, Blacksburg, VA 24061, USA. 3 Address Correspondence to: B. Merle Shepard, Clemson University, Coastal Research and Education Center, 2700 Savannah Highway, Charleston, South Carolina 29414, USA. 4 California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, California 95832, USA. 5 Department of Entomology, Soils and Plant Sciences, Clemson University, Clemson, South Carolina 29634, USA. 6 Department of Plant Protection, Bogor Agricultural University, Darmaga Campus, Bogor, West Java, Indonesia 16680. 7 The Polytechnic, Ho, Volta Region, Ghana. 8 International Institute of Tropical Agriculture, 08 BP 0932 Postal Cotonou, Republic of Be´nin. 9 Entomology Division, Bangladesh Agricultural Research Institute, Gazipur 1701, Bangladesh. 2
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years. They are actively extending their geographical ranges and they sometimes cause significant damage to important crops by direct feeding, and indirectly by deposition of honeydew that gives rise to sooty mold growth, which blocks light and air from the leaves and reduces photosynthetic productivity (Williams & Granara de Willink 1992). Contacts within host countries submitted additional samples, some of which were new country records. Neotropical species not recorded from Southeast Asia by Williams (2004) or Ben-Dov et al. (2001), and not recorded previously from West Africa by Ben-Dov et al. (2001), were regarded as new introductions. New country records are listed and discussed. These sapsucking pests, and in some cases their natural enemies, will continue to spread in Southeast Asia and West Africa due to movement of infested fresh plant material between countries, as happened in the spread of the papaya mealybug (Paracoccus marginatus Williams & Granara de Willink), the cassava mealybug (Phenacoccus manihoti Matile-Ferrero), and others (Neuenschwander 2003, Meyerdirk et al. 2004, Muniappan et al. 2006, 2008). New Country Records—Southeast Asia Bangladesh. Pseudococcidae: Paracoccus marginatus [Joydedpur, BARI campus, on Carica papaya (L.), coll. R. Muniappan & A.K.M. Rahman, 18.v.2009]. Cambodia. Coccidae: Ceroplastes ceriferus (F.) [Siem Reap, on Mangifera indica L., coll. R. Muniappan, 10.iv.2010]. Diaspididae: Thysanofiorinia nephelii (Maskell) [Phnom Penh, on Cassia sp., coll. R. Muniappan, 7.iv.2010]. Pseudococcidae: Paracoccus marginatus [Siem Reap, on Gardenia sp., Hibiscus sp., Plumeria sp., coll. R. Muniappan, 10.iv.2010; Phnom Penh, on C. papaya, coll. R. Muniappan, 5.iv.2010], Phenacoccus solenopsis Tinsley [Siem Reap, on Hibiscus sp., coll. R. Muniappan, 10.iv.2010], and Pseudococcus jackbeardsleyi Gimpel & Miller [Siem Reap, on Hibiscus sp., Plumeria sp., coll. R. Muniappan, 10.iv.2010]. Indonesia, West Java. Aleyrodidae: Aleurodicus dugesii Cockerell [Bogor, Cimanggu, on Hibiscus rosa-sinensis L., coll. P. Hidayat, 30.iii.2007; Cipanas, on Euphorbia pulcherrima Willd. ex Klotzsch, coll. R. Muniappan, 20.vii.2010]. Pseudococcidae: Phenacoccus manihoti [Bogor, Darmaga, on Manihot esculenta Crantz, coll. A. Rauf, 16.ix.2010] and P. solenopsis [Bogor, on Solanum lycopersicum L., coll. D. Sartiami, 23.vii.2010]. Other introductions to Indonesia recorded in the literature are Phenacoccus parvus Morrison, Nipaecoccus nipae (Maskell) and Pseudococcus jackbeardsleyi (Williams 2004). Philippines. Pseudococcidae: Paracoccus marginatus [Luzon, on C. papaya, coll. B. Cayabyab, viii.2008, immatures only; Manila, Pasay, on Plumeria sp., coll. R. Muniappan, 25.vii.2010; Nueva Eciija, Munoz, on Solanum melongena (Mill.) Dunal, coll. R. Muniappan, 26.vii.2010; Los Ban˜os, on Jatropha sp., coll. R. Muniappan, 29.vii.2010]; some of these samples were heavily parasitized, but the identity of the endoparasitoid is not known. Other recent introductions to the Philippines of neotropical origin are Dysmicoccus neobrevipes Beardsley, Phenacoccus madeirensis Green, Nipaecoccus nipae, and Pseudococcus jackbeardsleyi (Williams 2004). Thailand. Paracoccus marginatus [Bangkok, on Plumeria sp., coll. R. Muniappan, 3.iv.2010] and Phenacoccus madeirensis [Nakhon Ratjasima, Pak Chong, on M. esculenta, coll. A. Winotai, 27.iv.2010], whose likely presence in
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Thailand was mentioned by Winotai et al. (2010). Other recent introductions to Thailand recorded in the literature are D. neobrevipes, Phenacoccus solani Ferris, P. manihoti (Winotai et al. 2010), P. solenopsis (Hodgson et al. 2008), and Pseudococcus jackbeardsleyi (Williams 2004). New Country Records—West Africa Be´nin. Paracoccus marginatus [Hilacondji, on C. papaya, coll. G. Goergen, early 2010]. Ghana. P. marginatus [Nsawam Kede, on C. papaya, coll. M. Tamo`, xii.2009]. Togo. P. marginatus [Lome´, on C. papaya, coll. G. Goergen, ii.2010]. Species Discussions Aleurodicus dugesii (known as giant whitefly), collected from Indonesia by P.H. in 2007, was mentioned by Martin (2008), but it is recorded here in full for the first time. This is the second neotropical species of Aleurodicus to invade the region; the first was a spiraling whitefly, A. dispersus Russell, which began radiating westwards across the Pacific in the 1980s and is now widespread in Southeast Asia (Yu et al. 2007). Aleurodicus dugesii is likely to spread through the region in a similar way (Bellows & Meisenbacher 2000, Heu et al. 2004). The giant whitefly is a polyphagous species of Central American origin that prefers woody dicotyledonous hosts, including fruit trees and Hibiscus sp. (Evans 2008). It spread into the southeastern United States in the 1990s, reaching California in 1992 (Gill 2002) and Hawaii in 2002 (Heu et al. 2004). Like A. dispersus, it lays eggs on leaf undersides in spirals of white wax, and the immature stages produce long, glassy wax filaments that make infested leaves appear bearded. Adults of A. dugesii (3.0–4.5 mm long) are much larger than those of A. dispersus (1.8–2.5 mm long), have grey patterning on the forewing, and are very sedentary, whereas the forewing of A. dispersus has only one pale grey patch and the adults fly readily when disturbed. The giant whitefly can damage fruit trees and other crops by sap depletion and by fouling with sooty mold (Martin 2004), and the conspicuous nature of the infestations on ornamental plants is likely to cause public concern. In California and Hawaii, the giant whitefly is successfully controlled by parasitoids Idioporus affinis LaSalle & Polaszek (Hymenoptera: Pteromalidae), Encarsiella noyesii Hayat (Hymenoptera: Aphelinidae), and Entedononecremnus krauteri Zolnerowich & Rose (Hymenoptera: Eulophidae) (Heu et al. 2004, Zolnerowich & Rose 1996), so there is potential for classical biological control in Southeast Asia if the giant whitefly becomes a serious problem. In California, its preferred host is Hibiscus sp. (Malvaceae), so this whitefly might present a threat to cotton (also a member of Malvaceae), although it has not been recorded attacking cotton so far. Ceroplastes ceriferus, known as Indian wax scale, is native to South America (Waterhouse & Sands 2001). It is recorded here for the first time from Cambodia, although it is present in all of the neighboring countries (Ben Dov et al. 2001). It feeds on hosts belonging to over 50 plant families and is a pest of ornamentals and fruit trees (Ben-Dov 2010a); in the absence of natural enemies it could seriously damage several fruit crops in Cambodia.
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Paracoccus marginatus, the papaya mealybug, originated from Mexico (Williams & Granara de Willink 1992) and spread to the Caribbean Islands in 1994, South America in 1999, the Pacific Islands in 2002, and Southeast Asia in 2009 (Muniappan et al. 2008, Ben-Dov 2010b). In 2010, it was found in Be´nin (Goergen 2010) and Re´union (Germain et al. 2010). It is recorded here for the first time from Bangladesh, Cambodia, the Philippines, Thailand, Togo, and Ghana. In West Africa, P. marginatus has been collected along the road between Accra (Ghana) and the Be´nin border, including from Lome´ (Togo). Papaya mealybug is of major concern now in Ghana and is spreading rapidly. It was first seen on some farms near Accra a few years ago, and it has now reached Kumasi; it has also been seen in the Volta region. Papaya production in Ghana has seriously declined already in the major producing areas (the Greater Accra and Eastern regions). This polyphagous mealybug is known to attack plants belonging to 20 families, including numerous crops (Ben-Dov 2010b). Several countries in the Caribbean, South America, and the Pacific region have successfully implemented classical biological control to suppress populations of P. marginatus by introducing the endoparasitoids Acerophagus papayae Noyes & Schauff, Anagyrus loecki Noyes, and Pseudleptomastix mexicana Noyes & Schauff (Hymenoptera: Encyrtidae) from the USDA APHIS parasitoid-rearing laboratory in Puerto Rico (Meyerdirk et al. 2004, Muniappan et al. 2006). In Asia, Sri Lanka was the first country to import these parasitoids and to release them in May 2009; this brought about complete control of papaya mealybug by August 2009 (Anon. 2009). India imported the parasitoids and field-released them in October 2010 [J. Rabindra (National Bureau of Agriculturally Important Insects, Bangalore, Karnataka, India), personal communication]. On a visit to Java, Indonesia in July 2010, the IPM CRSP team found heavy parasitization of papaya mealybug by a fortuitously introduced parasitoid, A. papayae. Some of the papaya mealybug samples from the Philippines were also heavily parasitized but the identity of the parasitoid was unknown. While the samples of P. marginatus collected from Cambodia and Thailand showed no evidence of parasitism, it is possible that A. papayae or some other parasitoid may also become established; otherwise these countries should consider a classical biological control approach similar to that used in Sri Lanka, India, islands in the Pacific, and the Caribbean. Phenacoccus madeirensis, the Madeira mealybug, is of neotropical origin and is widespread in tropical South America, but was originally described from Madeira (Green 1923). It is now common in temperate areas in the USA, established in Micronesia, and is one of the most common species in tropical Africa (Williams & Granara de Willink 1992, Ben-Dov 2010c). It is continuing to expand its geographical range; Williams (2004) recorded it from Pakistan in 1997 and mentioned interceptions at U.S. plant quarantine facilities from the Philippines in 1999 and Vietnam in 1997. It was reported from Taiwan by Yeh et al. (2006). Here we record it from Thailand for the first time, on cassava. Madeira mealybug is highly polyphagous, feeding on members of 44 plant families, including many herbaceous crops, fruit trees, and ornamentals (BenDov 2010c). In California, it is common on ornamental plants in nurseries, and on sweet peppers (Capsicum annuum L.). Madeira mealybug has the potential to spread further in Southeast Asia. Phenacoccus manihoti, known as cassava mealybug, originated from central South America (Neuenschwander 2003) and it is infamous for the devastation it
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caused to cassava when it was accidentally introduced to equatorial Africa in the 1980s (Williams & Granara de Willink 1992). This species is oligophagous, feeding on members of nine plant families, but it strongly prefers cassava as a host (Neuenschwander 2003). It was first found in Southeast Asia (Thailand) in 2009, seriously damaging cassava, and has probably spread to Laos and Cambodia (Winotai et al. 2010). Here, we record it from Indonesia (Java) for the first time. This serious cassava pest is likely to spread further within the region; indeed, it may be present in other countries but has not been detected yet. In Africa, classical biological control of this mealybug has been very successful using the endoparasitoid Anagyrus lopezi De Santis (Hymenoptera: Encyrtidae). Thailand recently imported and released the same parasitoid (Winotai et al. 2010). Phenacoccus solenopsis, known as solenopsis mealybug, originated from the southwestern United States and was first described from New Mexico (Tinsley 1898). It was reported on cotton in Texas in 1992 and has since spread to South America, Asia, Africa (Wang et al. 2010), and reached Australia (Queensland) in early 2010 (Charleston & Murray 2010). Here, it is reported from Cambodia and Indonesia for the first time. The potential distribution of P. solenopsis was predicted by Wang et al. (2010) using CLIMEX eco-climatic model analysis, which indicated that it is likely to spread to many parts of the world. Phenacoccus solenopsis is a polyphagous and damaging pest, attacking plants belonging to over 50 families, including Cucurbitaceae, Fabaceae, Malvaceae, and Solanaceae (Hodgson et al. 2008). On tomatoes, it causes deformation and distortion of the terminal growth, twisting and curling of stems and leaves, and leaf wrinkling and puckering (Culik & Gullan 2005). Between 2006 and 2008, the solenopsis mealybug caused severe damage to cotton in Pakistan and India (Dutt 2007a,b) until a fortuitously introduced parasitoid, Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae), discovered in India in 2008, controlled the populations (Hayat 2009). The recent establishment of P. solenopsisis in Bangladesh, Cambodia, Indonesia, and Thailand could result in serious damage to vegetable and commercial crops unless A. bambawalei, or an equally effective parasitoid, is introduced. Pseudococcus jackbeardsleyi, known as the Jack Beardsley mealybug, is another polyphagous species of neotropical origin that attacks several vegetable and fruit crops and ornamentals. This insect was accidentally introduced to Hawaii in 1959, Kiribati in 1972, Tuvalu in 1976, and Papua New Guinea in 1979 (Gimpel & Miller 1996). The earliest record in Asia was from Singapore in 1958; it then spread to Malaysia in 1969, Indonesia in 1973, the Philippines in 1975, Brunei in 1979, Thailand in 1987, the Maldives, and Vietnam in 1994 (Williams 2004), and is here recorded from Cambodia for the first time. Pseudococcus jackbeardsleyi reached the Seychelles in 2003 (Germain et al. 2008), but has not yet been found in continental Africa. It is possible that local parasitoids may be keeping this insect under control in some countries. Thysanofiorinia nephelii, known as longan scale, probably originated from tropical eastern Asia, but has been spreading to other countries that produce longan fruit (Dimocarpus longan Lour.). Ben-Dov (2010d) documented that its host range is limited to members of four plant families, but the preferred host is longan. It has been recorded from Thailand (Ben-Dov 2010d), but this is the first
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record from Cambodia. The presence of this scale could impact commercial export of longan fruit due to plant quarantine restrictions. All of these invasive species are good candidates for classical or conservation biological control. Early detection, authoritative identification, and biological control of these pests are important in order to prevent or reduce serious economic losses, provide long-term control, and to decrease the likelihood of them spreading to other countries in the region. Acknowledgments This project was made possible by the United States Agency for International Development (USAID) Cooperative Agreement No. EPP-A-00-04-00016-00. This is technical contribution No. 5845 of the Clemson University Agricultural Experiment Station. We thank Dr. Gregory A. Evans (USDA, ARS) of the Systematic Entomology Laboratory, Beltsville, Maryland, USA, for confirming the identification of Acerophagus papayae from Indonesia.
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