Classical Biological Control of the Glassy-Winged Sharpshooter
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Biol Invasions (2008) 10:135–148 DOI 10.1007/s10530-007-9116-y ORIGINAL PAPER Engineering an invasion: classical biological control of the glassy-winged sharpshooter, Homalodisca vitripennis, by the egg parasitoid Gonatocerus ashmeadi in Tahiti and Moorea, French Polynesia Julie Grandgirard Æ Mark S. Hoddle Æ Jerome N. Petit Æ George K. Roderick Æ Neil Davies Received: 13 October 2006 / Accepted: 19 April 2007 / Published online: 25 May 2007 Ó Springer Science+Business Media B.V. 2007 Abstract The glassy-winged sharpshooter, Homa- surveys during the first year of their interaction in lodisca vitripennis Germar (=H. coagulata Say) French Polynesia (until mid-May 2006). The impact (Hemiptera: Cicadellidae), invaded Tahiti in 1999 of G. ashmeadi on H. vitripennis was extremely rapid and spread rapidly to the main island groups of and high. Parasitism of H. vitripennis egg masses by French Polynesia becoming an important pest. It G. ashmeadi has averaged 80–100% in Tahiti since threatened agriculture, native biodiversity, and the introduction of the parasitoid, and populations of created serious social and recreational problems. H. vitripennis nymphs and adults have decreased by Further, massive uncontrolled populations on Tahiti more than 90% since December 2005. Populations presented an elevated invasion threat to other South of H. vitripennis have been successfully maintained Pacific nations. In 2004, a classical biological control at this low level for more than 1 year. The same program against H. vitripennis was initiated in French results were obtained in nearby Moorea where the Polynesia using the highly host-specific egg parasit- parasitoid was probably spread by the unregulated oid Gonatocerus ashmeadi Girault (Hymenoptera: transport of plants infested with parasitized H. vitrip- Mymaridae). After risk assessment studies indicated ennis eggs. Population monitoring continues in order an acceptably low level of risk to non-target species, to determine if a stable equilibrium between the pest 13,786 parasitoids were released at 27 sites in Tahiti and the parasitoid has been reached. between May and October 2005. Here we present the results of G. ashmeadi and H. vitripennis population Keywords Classical biological control Á Impact assessment Á Parasitoid introduction Á Pest control Á Xylella fastidiosa J. Grandgirard (&) Á J. N. Petit Á N. Davies Richard B. Gump South Pacific Research Station, University of California, Berkeley, BP 244, 98728 Moorea, French Polynesia Introduction e-mail: [email protected] The glassy-winged sharpshooter, Homalodisca vit- M. S. Hoddle Department of Entomology, University of California, ripennis Germar (=H. coagulata [Say]) (Hemiptera: Riverside, CA 92521, USA Cicadellidae), invaded Tahiti, French Polynesia in 1999 (Grandgirard et al. 2006). It reproduced and G. K. Roderick spread very rapidly in French Polynesia and is Environmental Science, Policy and Management, Division of Insect Biology, University of California, currently found throughout the Society Islands Berkeley, CA 94720, USA archipelago and has spread to Nuku Hiva in the 123 136 J. Grandgirard et al. Marquesas archipelago (1,400 km northeast of Tahiti) Polynesia but also invaded Easter Island in 2005, and to Tubuai and Rurutu (600 km south of Tahiti) in likely as eggs transported on ornamental plants the Australs archipelago (Grandgirard et al. 2006; on flights from Tahiti (Sandra Ide, personal Petit et al. 2007). communication). Homalodisca vitripennis is native to the south- To minimize all of these problems, the feasibility eastern USA and northeastern Mexico (Triapitsyn of a classical biological control program against and Phillips 2000). Females lay their eggs within H. vitripennis using the exotic egg parasitoid Gonat- plant tissue, usually on the undersides of leaves of ocerus ashmeadi Girault (Hymenoptera: Mymaridae) shrubs and trees. Adults and the five nymphal stages was assessed. Classical biological control appeared are xylophagous and extremely polyphagous, having the most appropriate solution for controlling this pest been recorded feeding on more than 150 plant species in French Polynesia because this technology has the in 34 plant families (Hoddle et al. 2003). Due to the potential to: (1) significantly and permanently reduce low nutritional value of xylem, xylophages need to high pest population densities, (2) act without con- ingest large quantities of fluid. Consequently, H. vit- tinuous human assistance over a wide geographic ripennis can consume up to 100 times its body weight area, and (3) track H. vitripennis incursions into per day (Brodbeck et al. 1993) and copious amounts native habitats. The classical biological control of watery excreta are produced and continuously program against H. vitripennis with G. ashmeadi discharged as a result of prolific feeding. was initiated in French Polynesia in 2004 in collab- In its home and introduced ranges (e.g., California oration between the University of California (through USA), H. vitripennis is a major pest of agricultural, its Gump South Pacific Research Station on Moorea ornamental, and native plants because of its ability to and the Department of Entomology at Riverside) and vector the lethal xylem-dwelling plant bacterium, the French Polynesian Department of Agriculture. Xylella fastidiosa (Wells et al. 1987). In French Importantly, the program included non-target risk Polynesia, this insect also caused numerous problems assessment prior to parasitoid release (Grandgirard (Grandgirard et al. 2006). Firstly, it was a major et al. 2007a). public nuisance because: (1) massive densities of Gonatocerus ashmeadi is a solitary endoparasitoid feeding adults and nymphs generated high quantities attacking eggs of Proconiini sharpshooters (Cicadel- of excreta that literally rained from trees (hence its lidae: Cicadellinae: Proconiini) (Triapitsyn et al. common French name ‘mouche pisseuse’, the pissing 1998; Logarzo et al. 2003). It is native to southeastern fly), and (2) numerous flying adults invaded houses USA and northeastern Mexico (Triapitsyn et al. and shops at night attracted to the lights. Secondly, 1998) where it is a common and effective parasitoid thousands of adults and nymphs continuously feeding of H. vitripennis eggs. G. ashmeadi has several attri- year round were suspected of retarding plant growth butes that make it a promising candidate biological and causing declines in fruit production. Thirdly, control agent against H. vitripennis: (1) egg to adult H. vitripennis as a vector of X. fastidiosa represented development is about four times faster than that of a serious potential threat for Polynesian plants H. vitripennis (2 weeks vs. 2 months) (Pilkington and (agricultural, ornamental, native). While this bacteria Hoddle 2006a; Setamou and Jones 2005); (2) its sex has not been recorded in French Polynesia, many ratio is female-biased 1:3 (male:female) (Irvin and plants are asymptomatic reservoirs of the bacteria and Hoddle 2005); (3) G. ashmeadi attacks H. vitripennis could arrive in Tahiti (or could already be present) eggs on many different plant species in agricultural, with imports from infected regions (notably the urban, and wilderness areas (M. S. Hoddle, unpub- Americas). Finally, large uncontrolled H. vitripennis lished). In addition, it is the dominant parasitoid populations in French Polynesia represented an attacking invasive populations of H. vitripennis in invasion threat to neighbors and trading partners. southern California (Pilkington et al. 2005) and The immense population densities in French Polyne- tropical climates appear very favorable for its devel- sia made it impossible to contain this pest at ports and opment and reproduction (Pilkington and Hoddle live adults, nymphs, and eggs on plants were often 2006a, b). Rapid population suppression of H. vitrip- found in boats and planes leaving Tahiti. Conse- ennis by G. ashmeadi was observed in Hawaii, where quently, H. vitripennis not only spread within French this self-introduced parasitoid was found in late 2004 123 Engineering an invasion: classical biological control of the glassy-winged sharpshooter 137 (presumably arriving with host eggs). Initial parasit- Materials and methods ism estimates of H. vitripennis eggs in Hawaii were between 90 and 100%, and pest populations declined Parasitoid releases markedly and never reached the high levels observed in Tahiti (Bautista et al. 2005). Similar levels of Parasitoid rearing—G. ashmeadi was reared in the control of H. vitripennis by G. ashmeadi were quarantine facility of the Service of Rural Develop- expected in French Polynesia because of climatic ment in Papara, Tahiti. The quarantine colony at and habitat similarities. Papara was established in September 2004 with 400 Risk assessment studies for non-target cicadellid G. ashmeadi adults and parasitized H. vitripennis species in French Polynesia commenced in May 2004 eggs that were imported from the H. vitripennis with the compilation of an inventory of French biological control program being run at the Univer- Polynesia’s native cicadellid fauna. The risk of attack sity of California, Riverside. by G. ashmeadi was assessed by comparing native A nursery was established to provide plants for cicadellids with other known hosts for G. ashmeadi H. vitripennis oviposition and eggs were harvested by according to four criteria organized as a dichotomous picking leaves and presenting them in vials of water decision tree: (1) taxonomy (parasitoid host range is for parasitoids to attack.