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Home , Faaa, Gonatocerus ashmeadi, Gonatocerus triguttatus, Homalodisca, Paea, Papara

Invasion of by the Glassy-Winged , coagulata (: Cicadellidae): A New Threat to the South Pacific1

Julie Grandgirard,2,3 Mark S. Hoddle,4 George K. Roderick,5 Je´roˆme N. Petit,2 Diana Percy,2 Rudolph Putoa,6 Charles Garnier,6 and Neil Davies2

Abstract: The glassy-winged sharpshooter, Homalodisca coagulata (Say), is a major pest of agricultural, ornamental, and native plants. It is native to the southeastern and northeastern . Homalodisca coagulata was first recorded in (French Polynesia) in 1999. It reproduced and spread rapidly in French Polynesia and is currently found in almost all in the group (Tahiti, Moorea, , , Bora Bora, Tahaa, Maupiti), in Nuku Hiva in the Marquesas, and in Tubuai and Rurutu in the Australs. Tahiti and Moorea are the most heavily infested islands, where H. co- agulata populations have reached densities far exceeding those observed in Cal- ifornia (this pest invaded in the late 1980s) or in its native range. Major factors responsible for high population densities of H. coagulata in French Polynesia are permissive environmental conditions (mild climate and abundant year-round feeding and oviposition substrates), absence of host-specific natural enemies, intoxication of generalist predators that attack nymphal and adult stages, and limited competition for resources. Homalodisca coagulata causes sev- eral problems in French Polynesia: dripping excreta from high densities of feed- ing adults and nymphs affect outdoor recreation under trees and create a social nuisance, attraction of large numbers of flying adults to lights at night and col- lisions with people are severe annoyances, and large numbers of H. coagulata feeding on plants can cause impaired growth. The major concern for French Polynesia is the possibility of this pest acquiring and vectoring the lethal plant bacterium , which could have a disastrous impact on ornamental, agricultural, and native plants. Surveys are currently under way to detect X. fastidiosa in French Polynesia. Presence of large populations of H. coagulata in French Polynesia presents a major threat to agriculture and the biodiversity of South Pacific countries because this has clearly demonstrated a high invasion potential.

1 Financial support for research on H. coagulata was B. Gump South Pacific Research Station. Manuscript ac- provided by the French Polynesian government (Con- cepted 19 December 2005. vention no. 4.0328). Additional support came from the 2 Richard B. Gump South Pacific Research Station, University of California, Berkeley and Riverside; the University of California, Berkeley, BP 244, 98728, University of California Division of Agriculture and Nat- Moorea, French Polynesia. Resources; the California Department of Food and 3 Corresponding author: e-mail: julie@moorea Agriculture; and the Secretariat of the Pacific Commu- .berkeley.edu. nity. This paper is contribution no. 137 of the Richard 4 Department of Entomology, University of Califor- nia, Riverside, California 92521. 5 Environmental Science, Policy and Management, Division of Insect Biology, University of California, Pacific Science (2006), vol. 60, no. 4:429–438 Berkeley, California 94720. : 2006 by University of Hawai‘i Press 6 Service du De´veloppement Rural, BP 100, 98713, All rights reserved , Tahiti, French Polynesia.

429 430 PACIFIC SCIENCE . October 2006

Figure 1. The glassy-winged sharpshooter, Homalodisca coagulata (Say). Photo by Jack Kelley Clark, courtesy UC Statewide IPM Program.

The glassy-winged sharpshooter, Homalo- that require detoxification, and this may ac- disca coagulata (Say) (Figure 1), is native to the count for the extreme polyphagy of this southeastern United States and northeastern insect (Raven 1983). Due to the low nutri- Mexico (Triapitsyn and Phillips 2000). In tional value of xylem, xylophages need to in- the late 1980s this insect invaded California gest large quantities of fluid. Consequently, in the United States (Sorensen and Gill H. coagulata can consume up to 100 times its 1996), and by the mid-1990s populations in body weight per day (Brodbeck et al. 1993), Southern California had become widespread and copious amounts of watery excreta are and extremely pestiferous in agricultural and produced and continuously discharged as a urban areas (Pilkington et al. 2005). Homalo- result of prolific feeding. Females lay eggs disca coagulata exhibits high invasion potential, within plant tissue on the underside of leaves. having become successfully established in the Adults and the five nymphal instars can feed Pacific islands: French Polynesia in 1999 on more than 150 plant species in 34 plant (Secretariat of the Pacific Community 2002), (Hoddle et al. 2003). In its home Hawai‘i in 2004 (Hoover 2004), and Easter range and invaded areas, the major threat in 2005 (Sandra Ide, 2005, pers. posed by H. coagulata to agricultural crops comm.). Climate match modeling suggests and ornamental and native plants is its that many other areas of the world are highly ability to vector a xylem-dwelling bacterium, vulnerable to invasion by H. coagulata (Hod- Xylella fastidiosa (Wells et al. 1987), which dle 2004). causes a variety of lethal scorchlike diseases Homalodisca coagulata is xylophagous. Xy- in susceptible hosts (Hopkins and Purcell lem fluids lack defensive secondary chemicals 2002). Invasion of French Polynesia by Homalodisca coagulata . Grandgirard et al. 431

invasion of tahiti by homalodisca Department of Agriculture observations), coagulata and the Marquesas, where one island was found infested (Nuku Hiva) (November In French Polynesia, H. coagulata was first re- 2004, French Polynesian Department of Ag- ported in July 1999 on the windward island of riculture observations). On these recently in- Tahiti in the Society Islands fested islands, numerous nymphs and adults (Secretariat of the Pacific Community 2002). were found; therefore, the dates mentioned Nymphs and adults were found on one speci- do not correspond to the arrival of H. coagu- men of Lagestroemia speciosa in a private gar- lata but likely indicate that this pest had been den in the town of Arue, part of the present for several weeks or months and was metropolitan area of Papeete in the of noticed only after populations reached high Tahiti. In an attempt to prevent the spread of densities. It is possible that H. coagulata is this pest, the infested tree was treated with present on other islands in French Polynesia broad-spectrum insecticides before it was cut and has not yet been discovered. It is cur- down and destroyed. Homalodisca coagulata rently unknown if H. coagulata has invaded was not observed again in Tahiti until July– the Tuamotu group. August 2001, when large populations were Continued spread of H. coagulata in detected on numerous plant species in many French Polynesia is probably due to insuffi- different places in the metropolitan area of cient quarantine measures to prevent un- Papeete. The French Polynesian Plant Pro- wanted movement between infested and tection Department was alerted after nu- uninfested islands. Movement of plant mate- merous public complaints about the large rial is not controlled between islands within quantities of H. coagulata excreta raining the of Tahiti and its close from infested trees. Two possibilities exist island neighbor Moorea, which explains why for the discovery of this later infestation: (1) H. coagulata spread quickly from Tahiti to H. coagulata was not eradicated in July 1999, Moorea. Plants that are shipped from Tahiti or (2) subsequent accidental introductions to other more distant islands within French led to the 2001 outbreak. These hypotheses Polynesia are required to be dipped in insec- are not mutually exclusive and are difficult to ticides and fungicides. These dipping treat- distinguish without detailed genetic studies ments are unlikely to kill H. coagulata eggs (Davies et al. 1999a,b). It appears most likely because they are laid under the leaf epidermis that a permanent population of H. coagulata (Irvin and Hoddle 2004). However, insecti- was established in Tahiti in 1999 or earlier, cide residues on leaves could, on contact, kill probably due to infested ornamental plants H. coagulata nymphs that emerge from eggs bearing egg masses (this life stage is relatively to feed on treated plants. Since September immune to insecticide applications) imported 2004, heightened quarantine measures have from California. been implemented to prevent the movement Since it became established, H. coagulata of infested host plant material from invaded has spread rapidly within the Society Islands. islands into uncontaminated areas. Plants In 2001 it was found in Raiatea (Leeward Is- used for propagation are required to be defo- lands), in 2002 in Moorea, and small incipient liated, treated with insecticides, and fumi- populations of H. coagulata were discovered gated with methyl bromide. Fumigation with in the of Huahine and Bora methyl bromide is available only in Tahiti. Bora in 2003 and in Tahaa and Maupiti in Treated plants are then inspected for H. coag- 2005. At the end of 2004 and the beginning ulata eggs and rejected if eggs, nymphs, or of 2005, populations of H. coagulata were dis- adults are found. Flowers and foliage used covered outside the Society Islands in two for decorative displays are inspected for the other of French Polynesia sub- presence of H. coagulata eggs before being stantially distant from Tahiti: the Australs, moved between islands. If no eggs are found where two islands were infested (Rurutu and on ornamental flowers and foliage, they are Tubuai) ( January 2005, French Polynesian treated with an aerosolized insecticide. If H. 432 PACIFIC SCIENCE . October 2006

Figure 2. Numerous Homalodisca coagulata adults feeding on fruticosa in (Tahiti). coagulata eggs are found, shipments are re- urban areas at level to low-elevation areas jected or fumigated with methyl bromide. (Figure 2). Although apparently less abundant Despite these measures, H. coagulata adults at higher elevations, H. coagulata can be found or nymphs frequently are found alive inside in remnants of undisturbed native habitat on airplanes that move between islands in volcanic peaks exceeding 1,400 m above sea French Polynesia or out of French Polynesia level (Mount Marau, 1,493 m) ( J.G., pers. to other countries (e.g., , Aus- obs.). tralia, , and ) (M.S.H., J.G., and J.N.P., pers. obs.). factors favoring invasion in french To date, Tahiti and Moorea are the most polynesia heavily infested islands, which suggests that Moorea was infested before the nearby island The rapid proliferation and spread of H. coag- of Raiatea. In these islands, H. coagulata pop- ulata in French Polynesia can be explained by ulations have reached densities far exceeding five main factors: those observed in California or in its native (1) The general climate in French Polyne- range in the southeastern United States sia is ideal for H. coagulata reproduction (M.S.H., pers. obs.). Currently in Tahiti and (Hoddle 2004). French Polynesia has a humid Moorea, large H. coagulata populations are tropical climate (latitude 130–150 S), with readily found feeding and reproducing on a moderately high year-round temperatures wide variety of exotic and native plants in (annual average temperature 20.7C in Rapa Invasion of French Polynesia by Homalodisca coagulata . Grandgirard et al. 433

[Australs] to 27.4C in Takaroa [Marquesas]), gasterid. Female parasitoids attacked only one high relative humidity (annual average rela- to three eggs in a typical egg mass of seven to tive humidity 78% in Takaroa [Marquesas] ten eggs. Further, only haploid (male) eggs to 83% in Rikitea [Tuamotu-Gambier]), and were oviposited, indicating opportunistic par- high rainfall (annual average precipitation asitism and that H. coagulata eggs were as- 1,298 mm/yr in Nuku-ataha [Marquesas] to sessed to be of low quality. This absence of 2,664 mm/yr in Rapa [Australs]) (Laurent effective indigenous natural enemies probably et al. 2004). Moderate temperatures and had a direct influence on the establishment high rainfall ensure ideal year-round breed- and rapid spread of H. coagulata in French ing conditions for H. coagulata. It is estimated Polynesia. that in Tahiti there are six to eight over- (4) The invasion might have been favored lapping H. coagulata generations a year, com- by reduction of generalist preda- pared with two to three generations in tion due to intoxication by H. coagulata. Con- California and northern-central Florida trolled feeding experiments have revealed (United States). that some spiders in two species died after (2) French Polynesia offers numerous po- predation on H. coagulata. Mortality in both tential exotic and native host plants for H. co- the native crab spider Misumenops melloleitao agulata. In French Polynesia plant species are and the pan-Pacific orb-weaving spider Cyrto- diverse and abundant and provide year-round phora moluccensis appeared to result from lethal resources for feeding and egg laying. In par- intoxication, although no form of chemical ticular, high diversity of exotic plants and defense has been reported in H. coagulata.In commonness in urban areas ensure that H. co- both spider species, approximately half of all agulata has ideal conditions for feeding and spiders that attacked individual H. coagulata reproduction in areas where it is most likely nymphs or adults died. Field surveys revealed to be unintentionally moved. In addition to a decrease in M. melloleitao in areas where H. the underside of leaves of trees and shrubs, coagulata has become common. As H. coagu- H. coagulata egg masses are commonly found lata populations increase in size and distribu- on fern leaves (e.g., Polypodium sp.), grasses, tion on invaded islands in French Polynesia, sepals, skins of bananas, and occasionally on this insect will be increasingly encountered the upper surface of leaves. by these and other arthropod predators, rais- (3) Our surveys in French Polynesia indi- ing the possibility that declines in populations cate that there appear to be no effective of susceptible predator species could result natural enemies regulating H. coagulata popu- (Suttle and Hoddle 2006). lations. Surveys of H. coagulata egg masses on (5) Invasion by H. coagulata might have Tahiti and Moorea in 2003 indicated very low been favored because of weak competition levels of parasitism: less than 5% of the egg with other . Many of the isolated is- masses were attacked by parasitoids (Table lands in French Polynesia have relatively de- 1). The parasitoid species reared from H. co- pauperate arthropod faunas, which implies agulata egg masses was an unidentified platy- few competitors for invading insects. In par-

TABLE 1 Homalodisca coagulata Egg Survivorship

No. Eggs No. Eggs Killed No. Eggs No. Eggs No. Eggs Consumed by by Unidentified Successfully Examined Parasitized Predators Causes Hatched

2,586 32 (1.24%) 444 (17.17%) 50 (1.93%) 2,060 (80%)

Note: Data collected by M.S.H. over the period 3–9 September 2003 on Moorea, French Polynesia (246 egg masses were studied; 4% of collected egg masses were attacked). 434 PACIFIC SCIENCE . October 2006 ticular, the cicadellid fauna of French Poly- such as Metrosideros, Weinmannia, Dodonea, nesia seems impoverished, with few known Glochidion, Hibiscus, and , which have native species and a substantially greater no evolutionary association with this patho- number of exotic species that have established gen and may be extremely susceptible to in- accidentally (Osborn 1934). Consequently, fection. In the , the majority of competition by other proconiine cicadellids plants that succumb rapidly to X. fastidiosa in- is nonexistent because this tribe within the fection are those that have no evolutionary Cicadellidae is unique to the Americas and association with the bacterium (e.g., almonds, lacks naturally occurring representation in , European grape varieties, oleander, the South Pacific. peaches, and plums). Host plant surveys for Cumulatively, these five major factors (mild X. fastidiosa are under way using enzyme- climate, abundant year-round host plants for linked immunosorbent assay (ELISA) and feeding and oviposition, absence of effective polymerase chain reaction (PCR) technol- natural enemies, intoxication of generalist ogy, sentinel plant deployment (e.g., peri- predators, and weak interspecific competition) winkles [Vinca rosea] are highly sensitive to have facilitated invasion, a situation that is infection with X. fastidiosa), and culturing common for many successful invasive species of bacteria from potential host plants to de- (Shea and Chesson 2002). termine if X. fastidiosa is present in French Polynesia. the threat homalodisca coagulata Even in the absence of X. fastidiosa, H. co- poses to the south pacific agulata at the densities observed in French Polynesia is likely to have a negative impact The enormous populations of H. coagulata in on the exotic and indigenous flora. The huge French Polynesia are cause for concern and quantity of xylem fluid ingested by H. coagu- urgent remedial actions. Homalodisca coagulata lata nymphs and adults is suspected to weaken has a well-documented history in the United plants by inducing water-stress that leads to States of creating major agricultural problems leaf yellowing, defoliation, and growth re- that can result in substantial economic losses tardation. Physiological disorders caused by (California Department of Food and Agricul- populations of H. coagulata have been docu- ture 2004). The most serious threat to crops mented. Field studies by Hix (2004) and col- is a plant pathogenic bacterium, Xylella fastid- leagues have demonstrated that, for orange iosa, that is vectored by H. coagulata nymphs trees in California, H. coagulata is responsible and adults. Infection of plants with X. fastid- for changes in carbon and nitrogen metabo- iosa blocks the xylem, resulting in a variety of lism, which is indicative of tree stress, and leaf-scorch diseases, which can lead to the this pest is responsible for yield losses and re- death of plants (Hopkins and Purcell 2002). duced fruit size. In a more controlled experi- In California, disease is most devastating for ment, Andersen et al. (2003) demonstrated grapes, a crop worth approximately US$5 bil- that the quantity of nutrients and water de- lion per year (California Department of Food pleted by H. coagulata feeding over a 2- to 3- and Agriculture 2004). It is unknown if X. week period in Florida (part of the native fastidiosa is in French Polynesia. However, range in the United States) was substantial this bacterium is native to the Americas and but that effects on plant growth and metabo- it is possible that ornamental and agricultural lism were negligible. However, experimental plants imported to Tahiti from the Americas conditions used by Andersen et al. (2003) might be silent reservoirs, harboring bacteria were very different from what is observed without showing disease symptoms. The es- in Tahiti and California, where H. coagulata tablishment of H. coagulata with its ability to densities are orders of magnitude greater. In readily acquire and transmit X. fastidiosa could addition, in French Polynesia, unlike in Flor- result in disease epidemics affecting native ida and California, high densities of H. coagu- and ornamental plant species and agricultural lata feed continuously all year. Therefore, it is crops. Of particular concern are native plants, likely that H. coagulata has a substantial im- Invasion of French Polynesia by Homalodisca coagulata . Grandgirard et al. 435

Figure 3. Accumulation of ‘‘rain’’ excreted by Homalodisca coagulata nymphs and adults on leaves of Gardenia taitiensis. pact on plants in French Polynesia, especially after landing on exposed skin and presumably in Tahiti and Moorea. probing salt glands. Finally, H. coagulata has become a major The enormous density of H. coagulata in public nuisance in Tahiti. Excessive excre- French Polynesia represents an immediate ment produced by nymphs and adults results and important threat to other South Pacific in ‘‘rain,’’ earning H. coagulata the common nations and trading partners. At particular local name mouche pisseuse (‘‘pissing fly’’). risk are nations such as New Zealand and This ‘‘rain’’ makes it impossible to utilize with large and important agricul- shade under trees, and vehicles parked under tural industries that could suffer immense heavily infested trees are drenched in excre- losses if H. coagulata should invade via Tahiti ment that runs off vehicles and pools on and become established. Recent inspections roads and footpaths. Sharpshooter ‘‘rain’’ of cargo bins, hangars, and planes at the in- also creates an aesthetic problem by staining ternational airport in , Tahiti, found live leaves (Figure 3) and fruit. At night, huge and dead H. coagulata, indicating possible numbers of flying H. coagulata adults are at- stowaway sites via air transportation (M.S.H., tracted to lights, invading houses and busi- N.D., and G.K.R., unpubl. data). For exam- nesses and causing a considerable nuisance ple, adult H. coagulata could easily survive a by buzzing around and colliding with people 5-hr plane flight from Tahiti to New Zealand (Figure 4). In some instances, H. coagulata by flying into cargo holds and later escaping. adults have been alleged to ‘‘bite’’ people R.P. has noted reports of live H. coagulata 436 PACIFIC SCIENCE . October 2006

Figure 4. Numerous Homalodisca coagulata attracted to a light at night in (Tahiti). adults being discovered in planes from Tahiti gated. A review of potential control options that have landed in Japan. Dead H. coagulata was commissioned in 2003 by the French adults, that may have been alive at the begin- Polynesian Ministry of Agriculture. An ning of transit, have been found in planes ar- alliance between University of California riving in Cairns, Australia, that departed from (Berkeley and Riverside Campuses), the Uni- Tahiti and passed through versity of California Richard B. Gump South (M. Fletcher, 2005, pers. comm.). It is likely Pacific Research Station on Moorea, and the that the H. coagulata that invaded Easter Is- French Polynesian Agricultural Research and land came from Tahiti. Plant Protection Departments has guided the development of the classical biological con- biological control of homalodisca trol program against H. coagulata. In 2004, coagulata the biological control program using an egg parasitoid, ashmeadi (Hymenop- Consequently, there is an urgent and imme- tera: Mymaridae) (Figure 5), commenced diate need to control high-density popula- when populations of this parasitoid were es- tions of H. coagulata in French Polynesia. By tablished in a quarantine facility at reducing population densities many problems, (Tahiti). Gonatocerus ashmeadi is the most ef- both actual (human nuisance, and continued fective natural enemy attacking H. coagulata range expansion) and potential (widespread in California, hence its selection for this proj- vectoring of X. fasitidiosa), would be miti- ect. A second egg parasitoid, G. triguttatus, Invasion of French Polynesia by Homalodisca coagulata . Grandgirard et al. 437

Figure 5. Gonatocerus ashmeadi, an egg parasitoid of Homalodisca coagulata. Photo by Jack Kelley Clark, courtesy UC Statewide IPM Program.

may also be considered for release in French tinued spread of H. coagulata against the Polynesia, but release of G. triguttatus will potential conservation threat of introducing depend on the level of population suppres- exotic parasitoids to French Polynesia. Scien- sion achieved by G. ashmeadi. tific data will be paramount in guiding the A major requirement for classical biologi- decision to release exotic parasitoids for H. co- cal control of H. coagulata in French Polyne- agulata control. Carefully designed studies sia is consideration of environmental safety will identify potential environmental hazards (i.e., minimizing potential nontarget impacts and reduce uncertainties pertaining to un- on native cicadellid species). Particular atten- intentional nontarget impacts and levels of tion is being paid to the identification and expected control to be achieved by natural quantification of risk to native nontarget enemies of H. coagulata. fauna before the introduction of exotic para- sitoids commences. Currently, host risk as- acknowledgments sessment evaluations and native cicadellid surveys are under way to provide empirical We thank the University of California Re- data on the likelihood and magnitude of non- gents for the use of H. coagulata and G. ash- target impacts. Ultimately, the decision to re- meadi and G. triguttatus photographs. lease exotic parasitoids for biological control of H. coagulata rests with the French Polyne- Literature Cited sian government. The regulatory authorities must use a scientific approach to weigh the Andersen, P., B. Brodbeck, and R. Mizell. ecological, economic, and social risks of con- 2003. Plant and insect characteristics in re- 438 PACIFIC SCIENCE . October 2006

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