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Recent Invasive Hemipterans and Their Biological Control in Asia

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Recent Invasive Hemipterans and Their Biological Control in Asia RECENT INVASIVE HEMIPTERANS AND THEIR BIOLOGICAL CONTROL IN ASIA R. Muniappan Program Director, IPM CRSP, Virginia Tech 526 Prices Fork Road, Blacksburg, VA 24061, U.S.A. E-mail: [email protected] Abstract: In recent years, there is an increase in movement of invasive exotic species from one region of the world to others. Whiteflies and mealybugs constitute a major part of this invasion among the economically important arthropods. The spiraling whitefly, Aleurodicus dispersus, a native of the Caribbean and Central America established in Hawaii in 1978. Since then, it invaded the Pacific Islands in the early 1980s and then moved to Asia and Africa in the 1990s. It has been effectively controlled by the introduction of the parasitoid Encarsia? haitiensis and the coccinellid Nephaspis oculatus. Other neotropical species that are currently spreading in Asia is the giant whitefly Aleurodicus dugesii, that has established in Hawaii in 2002 and Indonesia in 2007 and the nesting whitefly, Paraleyrodes minei that has established in the middle east. The mealybugs that invaded old world tropics from the neotropics are the papaya mealybug Paracoccus marginatus, solenopsis mealybug Phenacoccus solenopsis, cassava mealybug Phenacoccus manihoti, Madeira mealybug Phenacoccus madeirensis and Pseudococcus jackbeardsleyi. Papaya mealybug was first collected in Mexico and it spread to the Caribbean in 1990s, the Pacific in early 2000 and Asia in late 2000. This mealybug has been effectively controlled by the introduction of the parasitoids Acerophagus papayae, Anagyrus loecki, and Pseudleptomastix mexicana. Solenopsis mealybug was first collected in New Mexico in 1897 and started to spread in early 1990s. Between 2005 and 2009, it caused severe damage to cotton in Pakistan and India. A fortuitously introduced parasitoid Aenasius bambawalei, discovered in the region successfully suppressed this pest. Recently this mealybug has been reported from Cambodia, Thailand and Indonesia. The cassava mealybug, originally from central South America, caused devastation of cassava in the 1980s when it was accidentally introduced to equatorial Africa. It was reported from Thailand, Cambodia, and Laos in 2009, and Indonesia in 2010. This mealybug has been successfully controlled in Africa by introducing the parasitoid Anagyrus lopezi. Madeira mealybug is also of neotropical origin and widespread in tropical South America. It was reported from Pakistan in 1997, Taiwan in 2006 and Thailand in 2010. Pseudococcus jackbeardsleyi, another neotropical species was introduced to Singapore in 1958, Hawaii in 1959, the remainder of the Southeast Asia in 1970s and to Maldives in 1994. It is possible that local parasitoids are keeping Madeira mealybug and P. jackbeardsleyi under control in some of these countries. Introduction. The globalization and the concomitant increase in international travel and commerce are directly correlated to the resultant enhancement in introduction and spread of exotic invasive species. Often species introduced without their natural enemies from the new world to old world and vice versa become invasive in the countries into which they were introduced. Invasive species cause loss of biodiversity, modify the habitat and cause extensive environmental and economic harm (Fish et al., 2010). In the recent years, several species of economically important arthropods have been introduced to different countries and the rate of introduction in the tropics is much higher than in the temperate regions. For example, Hawaii and Florida experience for more number of introductions per year than the other states in United States of America. Losses caused by invasive arthropods alone account for several billions of dollars per year. Invasive species have lead to abandoning of cultivation of crops and associated economic consequences in many parts of the world. From 2005 to 2009, cultivation of cotton in Pakistan and India came under severe stress because of the accidentally introduced pest, Phenacoccus solenopsis Tinsley. This paper outlines some of the hemipteran insect pests that are invading Asia from the neotropics and the classical biological control programs adopted for their suppression. Whiteflies (Hemiptera: Aleyrodidae) The spiraling whitefly, Aleurodicus dispersus Russell It is native to the Caribbean region and Central America (Waterhouse and Norris, 1989). It was first recorded from Florida in 1957. In the Pacific, it was reported from Hawaii (1978) and Guam and other islands (1981 and afterwards) (Waterhouse and Norris, 1989). In Asia it was reported in the Philippines (1981), Indonesia (1991), India (1993), Bangladesh (1997), and China (2006) (Yu et al., 2007). It was accidentally introduced to Nigeria around 1992 and to rest of the West Africa afterwards (Akinlosotu et al., 1993; Legg et al., 2003). It reached Kenya in 2010 (Mware, 2010). It is a polyphagous pest and it is known to attack over 481 species of plants in India (Srinivasa, 2000). Damage was caused by direct feeding as well as reducing photosynthetic surface by nurturing sooty mold through copious production of honeydew. In India, Saminathan and Jayaraj (2001) found that the cotton variety SVPR 2 was most susceptible as it harbored 34 nymphs and 36 adults per plant and 62% of the plants were infested. In contrast, the variety MCU 9 was most tolerant to A. dispersus, with 14 nymphs and 14 adults per plant with a total infestation level of 21% of the plants. When A. dispersus became a serious problem, Hawaii Department of Agriculture conducted exploratory work in the Caribbean and introduced three coccinellids and two aphelinid parasitoids in 1979. Of these, the coccinellid Nephaspis oculatus Blatchley) (=N. amnicola) (Coleoptera: Coccinellidae) and the parasitoids Encarsia ?haitiensis Dozier and Encarsia sp. (Hymenoptera: Aphelinidae) were found to be effective in suppressing the whitefly population. When A. dispersus spread to other Pacific Islands in the 1980s, E. ?haitiensis and N. oculatus were introduced from Hawaii (Waterhouse and Norris, 1989). The parasitoids Encarsia guadeloupae Viggiani and E. ?haitiensis were fortuitously introduced into Asia and Africa and they seem to control this pest effectively (Legg et al., 2003; Mani, 2010). In countries wherein A. dispersus established without its natural enemies, introduction of E. guadaloupae, E. ?haitiensis and N. oculatus should provide satisfactory control of this pest. The giant whitefly, Aleurodicus dugasii Cockerell This whitelfy is of Central America in origin and it has spread to Texas (1991) California (1992), Louisiana and Florida (1996), and Hawaii (2002) (Gill 1992; Hodges, 2004; Heu et al., 2004). It was reported from Java, Indonesia in 2008, a first report from Asia (Muniappan et al., 2011). It is likely to spread through Asia similar to A. dispersus. Giant whitefly is polyphagous and it prefers woody dicotyledonous hosts including cotton, fruit trees, and ornamental plants. Adults and nymphs damage plants by sucking sap through their needle-like mouthparts. Heavy infestations usually result in decline in plant growth. When the giant whitefly became a problem in southern California, two entomologists from the University of California at Riverside, explored Mexico for natural enemies in 1997. Two parasitoids, Idioporus affinis LaSalle and Polaszek (Hymenoptera: Pteromalidae) and Encarsiella noyesii Hayat (Hymenoptera: Aphelinidae) and released in 1997 and 1998 (Bellows and Meisenbacher, 2000). Another parasitoid, Entedononecremnus krauteri Zolnerowich and Rose (Hymenoptera: Eulophidae) was found in Texas and it has also been distributed to California and Florida in 1995 (Zolnerowich and Rose, 1996). In addition, a local parasitoid Encarsia hispida De Santis (Hymenoptera: Aphelinidae) was also found attacking early instars this whitefly. In Hawaii the parasitoid, I. affinis was introduced fortuitously from California in 2003 and it has kept this whitefly under control. The nesting whitefly, Paraleyrodes minei Iaccarino It is another whitefly of neotropical origin was accidentally introduced to California (1984) (Bellows et al.1998), Syria (1989), Israel (1993), Turkey (1994), Lebanon (1999), Benin (2000), and Spain (2006). It has been recorded on 37 host plants belonging to 21 families in Syria (Mohammad and Abboud, 2001). No classical biological control program has been attempted for this whitefly possibly because of control by local natural enemies. Mealybugs (Hemiptera: Pseudococcidae) Papaya mealybug, Paracoccus marginatus Williams and Granara de Willink The papaya mealybug is a native of to Mexico and/or Central America (Miller et al., 1999) and it was described in 1992 from the specimens collected in Mexico. In 1997 it appeared in St. Martin Island and later spread to rest of the Caribbean Islands, Florida and some countries in South America. In 2002, it was reported in the Pacific Islands (Meyerdirk et al., 2004, Muniappan et al., 2006) and in 2008 in Indonesia, India, and Sri Lanka (Muniappan et al. 2008). In 2009, it was reported from Bangladesh and Maldives and in 2010 in Cambodia, Philippines and Thailand (Muniappan et al., 2011). Papaya mealybug has a wide host range of over 60 species of plants including Annona squamosa, Carica papaya, Hibiscus rosa-sinensis, Ipomea spp., Gossypium spp., Jatropha sp., Manihot esculenta, Parthenium hysterophorus, Sida acuta, Acalypha indica, Cassia sericea and others (Meyerdirk and Kauffman, 2001; Shylesha et al., 2010). Affected young leaves crinkled, the shoots become stunted
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