Homalodisca vitripennis (glassy winged sharpshooter)

H. vitripennis is a large insect (about 13 mm). It is generally brown to black but the underside of the abdomen is whitish. The upper aspect of the head and thorax is brown or black with numerous ivory to yellowish spots. These spots allow H. vitripennis to be easily distinguished from its close relative, the native Californian smoke tree sharpshooter (Homalodisca lacerta), which has pale, wavy lines instead of the spots. The sausage-shaped eggs are laid side-by-side in masses averaging 10 to 11 eggs. The egg masses appear as greenish water blisters beneath the leaf. They are elongate, with the individual eggs running transversely across the mass. The nymphs are dark grey (first and second stage) to grey (third to fifth stage). The cast skin from the final nymphal moult to the adult often adheres to the stem or leaf surface (Phillips, 1998).

H. vitripennis is primarily a south-eastern US species and is abundant from eastern Texas to northern Florida, including the states of Louisiana, Alabama, Mississippi, Georgia, South Carolina and the southern parts of North Carolina and Arkansas (Turner and Pollard, 1959). Populations of the pest decrease considerably in central and southern Florida (Hoddle et al., 2003) and central Texas. It appears to be rare in the states of Tamaulipas and Nuevo Leon of north-eastern Mexico (Triapitsyn and Phillips, 2000). Due to an apparent accidental introduction in 1999 (most probably from California), it has recently become a problem pest of ornamentals and native plants in French Polynesia (NHM Entomology enquiry 2001-1068) and crops and ornamentals in southern California (Blua et al., 1999) with most recently established populations in the central and northern parts of that state.

The greatest threats are to regions with mild winters where one or more of the following crops are grown: grapes, citrus, almond, stone fruits (Prunus spp.), coffee, oleander, or where tree species potentially affected by leaf scorch diseases occur. There is an internal quarantine against movement within the state of California from areas of known infestation to central and northern California. Australia has imposed a quarantine against this insect as no vectors of Pierce's disease are known to exist there. Tahiti poses a major infestation epicentre for the south Pacific and planes and cargo bins should be disinfested before leaving the country. Dead sharpshooters have been found in cargo bins. Large numbers are attracted to hangar lights at night and yellow on the sides of planes may attract flying sharpshooters, which will enter open plane doors.

The implementation of phytosanitary measures to curb unwanted incursions needs to be scientifically justifiable if restrictions are to be in accordance with Sanitary and Phytosanitary Agreement of the World Trade Organization and the International Plant Protection Organization. Consequently, if it can be demonstrated that a particular invader cannot extend its range and establish transient populations in an area under consideration then exclusion is not technically justifiable.

The following steps should be considered to mitigate invasion by H. vitripennis and the subsequent spread of diseases caused by X. fastidiosa. These ideas are common sense but require a coordinated research effort and cooperation between governments, scientists, legislators, growers and the public:

- Exotic plants from the Americas, which could potentially harbour X. fastidiosa, need to be identified and a list prepared of potential symptomless reservoir species from surveys.

- Intensive surveys of plants identified as potential X. fastidiosa reservoirs should be conducted to determine whether they harbour the bacterium. Plant species testing positive for X. fastidiosa should be eradicated and their continued propagation, distribution and importation banned.

- Potential pathways that could permit H. vitripennis to reach other countries from French Polynesia and the USA, in particular ornamental plants from California and Florida, need to be identified and intensively monitored. Similarly, potential movement pathways for X. fastidiosa out of California, Florida, Taiwan and Kosovo need to be determined and monitored.

- Scientists need to be consulted to identify and list native and exotic xylophagous insect species (i.e., hemipterans in the families Cicadellidae (subfamily Cicadellinae; tribes Cicadellini and Proconiini) Cercopidae and Cicadidae which vector X. fastidiosa (Purcell, 1989, 1997)) that have invasion and X. fastidiosa vectoring potential. Potential invasion pathways for these insects need to be determined and monitored to contain and eradicate early incursions.

- Studies exploring the potential threat posed by X. fastidiosa to native plants in recently invaded ranges should be investigated. This may be relatively easy to do as native plants in invaded areas may be grown as ornamentals in California and Florida and cooperative studies between scientists in the USA and other countries could be initiated to study the susceptibility of native flora to X. fastidiosa and their attractiveness to H. vitripennis.

- Further investigation of the effect of cold temperatures on the survival and infectivity of different strains of X. fastidiosa is required to help predict the likelihood of establishment in areas currently considered 'too cold' for this bacterium. Public education programmes need to be strengthened to highlight the threat that invasive pest species pose to agriculture and wilderness areas, and the unacceptable risks associated with 'sneaking in' plant material needs to be re-inforced with severe fines.

Adult glassy-winged sharpshooters are strong fliers and can move rapidly from plant to plant. Nymphs are wingless and cannot fly but can distribute themselves by walking and jumping through the canopy or dropping from plants and walking to new hosts. Most rapid and long distance movement is as viable egg masses in nursery stock of either crop or ornamental plants.

As H. vitripennis continues to expand is range within California following its accidental introduction (ca 1989), both the ovipositional and feeding host lists continue to expand, primarily within ornamental plant species grown in nurseries or landscape gardens. As it is a xylem feeder, it circumvents secondary plant defence chemistry found in phloem sap and, as a result, it appears to be able to feed on most plant species. The high volume of xylem fluid intake required limits its survival to situations in which continued contact with a living host is possible. Only the egg stage is capable of survival for 2 or 3 weeks on excised plant foliage as long as it is kept fresh and moist.

H. vitripennis attacks plants in the following families: Aceraceae, Agavaceae, Amaranthaceae, Anacardiaceae, Apocynaceae, Aquifoliaceae, Araceae, Araliaceae, Asclepiadaceae, Asteraceae, Begoniaceae, Berberidaceae, Betulaceae, Bignoniaceae, Buxaceae, Caesalpiniaceae, Caprifoliaceae, Caprifoliaceae, Casuarinaceae, Celastraceae, Chenopodiaceae, Clusiaceae, Combretaceae, Convolvulaceae, Cupressaceae, Cycadaceae, Eleagnaceae, Ericeae, Euphorbiaceae, Fabaceae, Ginkoceae, Graminaceae, Hamamelidaceae, Iridaceae, Juglandaceae, Lamiaceae, Lauraceae, Liliaceae, Logaiaceae, Lythraceae, Magnoliaceae, Malvaceae, Meliaceae, Moraceae, Myoporaceae, Myrtaceae, Nyctaginaceae, Nyssaceae, Oleaceae, Onagaaraceae, Phytolaccaceae, Pinaceae, Pittospaceae, Platanaceae, Poaceae, Podocarpaceae, Polypodaceae, Proteaceae, Rosaceae, Rubiaceae, Rutaceae, Salicaceae, Sapindaceae, Sapotaceae, Saxifragaceae, Theaceae, Ulmaceae and Vitaceae.

H. vitripennis is native to the subtropical gulf states of south-eastern USA, in areas with a high water table where wild hosts produce the luxuriant growth necessary to sustain this prodigious xylem feeder. Its native range also includes the more arid regions of southern Texas and north-eastern Mexico, especially irrigated habitats such as landscape gardens and citrus orchards. After the recent introduction and spread of H. vitripennis in California, it has become extremely abundant on citrus and several ornamental and native plant species in southern parts of the state (Sorensen and Gill, 1996). Despite originating in a humid, subtropical region H. vitripennis can become abundant in Mediterranean climates if plants receive adequate irrigation and winter temperatures are not to severe.

H. vitripennis is a stem feeder and leaves no visible symptoms of its feeding other than a white, powdery, dried excrement on plant surfaces.

Feeding causes no visible signs of damage, even though the insect consumes hundreds of times its body weight per day in xylem fluid. Most non-xylem-feeding leafhoppers produce a sugary or particulate excrement, but the excrement of xylem feeders is watery, high in ammonia and dries to a fine, whitish powder which can cover the stems, foliage and fruit when the insects are abundant (Phillips, 1998). High densities of feeding sharpshooters excrete enough waste product to cause a 'rain', which falls from the trees; this rain can easily be seen on sunny days and can be felt on the skin. This phenomenon is particularly acute in Tahiti where puddles form on roads and side walks as result of sharpshooter rain.

Egg masses are usually laid into recently expanded foliage. Older foliage will contain the distinctive scars left after the eggs have hatched. When populations are more abundant, egg masses can be laid into the rind of immature fruits of crops such as citrus and melon. Old hatched egg masses appear as grey or tan scars on surface of the rind (Blua et al., 1999).

H. vitripennis most closely resembles the native California smoke tree sharpshooter Homalodisca lacerta (Gill, 1994; see Morphology).

Like other sharpshooter species, H. vitripennis is capable of transmitting the bacterium Xylella fastidiosa, the causal agent of numerous leaf scorch diseases (Alderz and Hopkins, 1979), which cause stunting, a general debilitation of the host and irreversible water stress symptoms.

H. vitripennis can survive in arid areas as long as there is sufficient irrigation to keep host plant xylem at a suitable quality that is acceptable to feeding adults and nymphs. Irrigation of agricultural lands, botanical gardens and urban areas has greatly facilitated invasion of this pest into areas that would otherwise be unsuitable. CLIMEX modelling has indicated that cold temperatures in states north of California in the USA will exclude establishment of H. vitripennis. CLIMEX modelling also indicated that tropical habitat in the South Pacific will be ideal for H. vitripennis and this has been confirmed by the recent establishment (1999) on Tahiti and Moorea in French Polynesia. Furthermore, H. vitripennis has been found feeding on native plants at the highest altitudes in French Polynesia.

The glassy-winged sharpshooter (GWSS) produces two generations a year in southern California. After a peak in adult activity during the winter months, oviposition begins in late winter and early spring (February/March), peaking in May. Adults live about 2 months. They lay their small, sausage-shaped eggs side-by-side in masses, each mass averaging 10 to 11 eggs. The eggs are laid just under the lower leaf epidermis of host plants. Egg masses can range from a single egg to masses containing as many as 27 eggs. Egg masses appear as greenish water blisters beneath the leaf. They are elongated with the entire mass being sausage-shaped, with the individual eggs running transversely across the mass. When viewed from above, they are marked by a yellowish or chlorotic, elongated blotch. Eggs are often covered with a white, chalky material, brochosomes, produced from malpighian tubules and exuded through modified pores towards the rear of the abdomen. Laboratory investigations suggest that the function of brochosome deposition is to interfere with parasitoid activity by increasing grooming rates for parasitoids compared to egg masses lacking brochosomes. The nymphs hatch in about 2 weeks and proceed to feed on leaf petioles or small stems, while progressing through five moults before becoming winged adults. A second peak in adult activity occurs in the summer during July and August. Peak oviposition in these first generation adults occurs in August. After the eggs have hatched, the old egg mass blister appears as a tan to brown scar. Oviposition is greater in native laurel sumac, macadamia, lemon and the ornamental Pittosporum spp. than in most other oviposition hosts. There are many hosts on which this insect feeds but does not lay eggs (Phillips, 1999b). In Tahiti, H. vitripennis is multivoltine with multiple overlapping generations. At night large numbers of adult H. coagulata are attracted to lights around houses, shops and airport hangers. This insect has been reported to 'bite' people when adults land on skin and probe sweat glands with mouthparts. Furthermore, 'sharpshooter rain' (excessive fluid excretion from large populations feeding in trees) is a major public nuisance in Tahiti and has led to the decline and partial defoliation of ornamental street trees.

A significant proportion of GWSS egg masses were parasitized by the mymarid wasp, Gonatocerus ashmeadi, a key natural enemy of H. vitripennis (Triapitsyn and Phillips, 1996). G. ashmeadi was previously reported from eggs of Homalodisca lacerta on citrus and other plants in California (Huber, 1988) and from H. vitripennis eggs in Georgia (Turner and Pollard,1959). Triapitsyn et al. (1998) reviewed the mymarid parasitoids of H. vitripennis in the south-eastern USA and southern California. Genetic, cross breeding and morphological studies suggest G. ashmeadi is native to the gulf state areas of the USA and Mexico and most likely invaded California along with H. vitripennis.

Since 1996, four species of mymarid egg parasitoids have been recovered from GWSS egg masses in southern California. Endemic species of parasitoids (Gonatocerus) have consistently been recovered during field biology studies of the GWSS in commercial citrus orchards in Ventura County, California. Of four species recovered (G. ashmeadi, G. morrilli, G. incomptus and G. novifasciatus), G. ashmeadi was the predominant species, accounting for more than 95% of all recorded parasitism. G. morrilli was the most abundant of the other three, but primarily occurs in July. G. incomptus has only been recovered in April and G. novifasciatus in June. Annual fluctuations in parasitoid activity, measured by yellow sticky traps and GWSS egg collections, are synchronized with the two periods of GWSS oviposition each year. Parasitism of first generation GWSS egg masses in the late winter to spring, is very low compared to that of second generation egg masses from late summer to early autumn. First generation GWSS egg mass parasitism was higher in 1999 than in the previous 2 years. Despite rates of parasitism averaging 40% and ranging from 10 to 85% on second generation GWSS egg masses, the overall percentage parasitism for the year was only about 10% in lemons and 15% in oranges. With these rates of parasitism, GWSS populations continue to increase in the citrus orchards of Ventura County. In April 1999, an exploratory trip was undertaken to the states of Nuevo Leon and Tamaulipas in north-eastern Mexico to search of a more effective parasitoid of first generation GWSS egg masses. Another mymarid, G. triguttatus was recovered from GWSS eggs in both lemon and peach foliage (Triapitsyn and Phillips, 2000). This was the first GWSS host record for this species, which has subsequently been imported from Mexico in April, 2000 through quarantine at UC Riverside and into California citrus. Mass rearing and release of this parasitoid is planned for 2001 with funding from the California Department of Food and Agriculture (CDFA). Additionally, G. fasciatus, a gregarious parasitoid has been recovered from H. coagulata egg masses in Louisiana. This parasitoid has been mass-reared and released in California by the CDFA (Triapitysn et al., 2003)

Although endemic mymarid parasitoids have quickly exploited the almost unlimited supply of egg masses available in southern California citrus orchards resulting from very large populations of GWSS, parasitism rates calculated as total egg load over the year are rather low. The presence of very few fresh GWSS egg masses during the winter months in citrus and other evergreen hosts probably restricts the ability of the egg parasitoids to survive the winter at high enough population levels to suppress first generation GWSS egg masses in the spring. Low levels of parasitism of first generation GWSS eggs allow GWSS populations to grow exponentially in the second generation. The recently introduced G. triguttatus may improve parasitism rates in the spring, as GWSS populations are very low in Mexico, where this mymarid species was recovered during the spring. A similar prospecting strategy recovered G. fasciatus from Louisiana, where this parasitoid is most common early in the season and is later replaced by G. ashmeadi. Release of G. fasciatus in California is an attempt to increase mortality of GWSS eggs in the spring generation. Although current rates of GWSS egg parasitism probably buffer the impact of H. vitripennis as it expands its range, biological control is expected to significantly reduce densities of H. vitripennis. However, other strategies will be required to manage the H. vitripennis-Xylella problem which is problematic even in areas where GWSS is native and under excellent biological control.

Biological control is being considered as a management option for GWSS in Tahiti. The major concern here is to reduce GWSS densities to significantly lower levels thereby reducing the likelihood of this pest continuing its spread through the South Pacific.

In economic terms, grapes are worth US $3.2 billion and associated economic activity exceeds US $33 billion in California. In addition, crops such as almonds and stone fruit have been valued at US $897 million and US $905 million, respectively, and are at risk from strains of X. fastidiosa, which cause disease in these host plants (CDFA, 2003). The H. vitripennis-Xylella fastidiosa combination could potentially have a severe and adverse affect on California's agricultural industries and subsequently on the state's economy. In 2002, the state of California and primary producers incurred additional economic costs resulting from spread containment activities such as inspections of nursery stock being moved out of southern California, and shipments of bulk grapes and citrus from H. vitripennis-infested counties (CDFA, 2003). There are currently in excess of 70 research programmes on H. vitripennis or X. fastidiosa. Because of the serious nature of this problem and the vast sums of money at stake, the National Academy of Sciences (NAS) of the USA has subjected these programmes to evaluation and assessment (CDFA, 2003). The NAS has a mandate requiring it to advise the Federal Government on scientific and technical matters.

Theoretically, if H. vitripennis egg masses arrived on plants in a new area the nymphs that hatch from these eggs would not have X. fastidiosa because the bacterium needs to be acquired from the xylem of infected plants via feeding. Furthermore, X. fastidiosa is lost from sharpshooter mouthparts each time juveniles moult and bacteria must be re-acquired through feeding on infested host plants (Almeida and Purcell, 2003). Consequently, adult sharpshooters are permanently infected with X. fastidiosa but adult age affects transmission efficiency (Almeida and Purcell, 2003). Because a wide variety of ornamental plants have been imported into various countries from the Americas, it is probable that reservoirs of X. fastidiosa exist in countries lacking H. vitripennis or native sharpshooters that can vector the disease. Potential host plants may harbour X. fastidiosa without exhibiting disease symptoms (Hopkins and Purcell, 2002). Consequently, it may be relatively easy for H. vitripennis to acquire X. fastidiosa in new countries after it establishes, proliferates and spreads by feeding on symptomless hosts infected with this bacterium. Consequently, H. vitripennis may irrevocably change the ecology and movement of X. fastidiosa in wilderness areas as this polyphagous insect could be exposing a variety of novel native hosts to a pathogen with which these plants have had no evolutionary history.

Declining productivity for agricultural commodities in California due to GWSS-Xylella could have major social ramifications as job losses are incurred and the economic base for rural communities declines. The potential impact on grape production in California could have a major impact on the economic trajectory of this US state. In Tahiti, GWSS numbers are so extraordinarily high that they constitute a major social problem because of sharpshooter 'rain' falling from trees, which can drench parked vehicles and wet people resting or walking under infested trees. Large numbers of adults are attracted to lights at night and become trapped indoors where they die forming large piles of cadavers. The erratic flight of the insect around lights in public areas at night can result in constant bombardment of people and annoying and persistent tapping on windows as the GWSS collide with glass. Occasionally, GWSS will 'bite' people as they probe sweat glands after landing on expose skin.

Yellow sticky traps are commonly used for surveillance and detection. Colour preferences for attraction to H. vitripennis are not well known, but it will fly to yellow. On warm nights it is attracted to black and incandescent lights. Active stages may be found by searching plant stems. Fresh egg masses are found on the underside of recently matured foliage (older foliage should be avoided). Active stages can be easily detected by placing a tarpaulin under the suspected host plant, at temperatures below 15°C, and striking the plant vigorously. A sweep net placed over the foliage can be used in a similar manner (Phillips, 1999a; Varela et al., 2001).

Phytosanitary measures can be used to slow dispersal and range expansion of H. vitripennis.

Chemical control practices are not generally necessary as suppression of the vector rarely leads to a significant reduction in disease incidence. Chemical control is only recommended in instances where the objective is to slow the dispersal of the vector to new ranges. There are no prescribed control programmes within the native range of H. vitripennis in the south-eastern USA. The exception is in citrus in southern California, where newly planted orchards, up to 3 years of age, can sustain vigour/growth losses due to high populations (50-100 insects/plant) during the hot, dry summer months. Evaporative demand coupled with xylem fluid losses resulting from insect feeding can result in wilt symptoms at midday. Sustained high populations can also result in losses in yield and fruit quality. In such cases, chlorpyrifos can be used, with limited residual activity, to kill active stages. The application of imidicloprid as a systemic insecticide can suppress the population by 95% for up to 5 months. Field trials in California suggest that pyrethroids and synthetic neonicotinoids may be the most suitable for use in integrated pest management programmes, and combinations and rotations of products may be necessary to minimize resistance development (Akey et al., 2001; Bethke et al., 2001).

Biological control from indigenous mymarid egg parasitoids can account for 20-40% of mortality in the spring generations in California. The second generation of egg masses in summer experiences >95% parasitism and ~100% of eggs in discovered egg masses are parasitized. The mass production and release of parasites is currently under investigation as a control tactic. However, given the difficulty of mass rearing GWSS year round it is unlikely that seasonal augmentative releases of mass-reared mymarid parasitoids will be economically feasible, or that the parasitoid would be produced in high enough numbers to have an impact.

Sweep net sampling and yellow, sticky cards or ribbons can be used for field monitoring of populations or new infestations.