Successful Spread of a Biocontrol Agent Reveals a Biosecurity Failure: Elucidating Long Distance Invasion Pathways for Gonatocerus Ashmeadi in French Polynesia
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BioControl DOI 10.1007/s10526-008-9204-7 Successful spread of a biocontrol agent reveals a biosecurity failure: elucidating long distance invasion pathways for Gonatocerus ashmeadi in French Polynesia Je´roˆme N. Petit Æ Mark S. Hoddle Æ Julie Grandgirard Æ George K. Roderick Æ Neil Davies Received: 30 August 2008 / Accepted: 24 November 2008 Ó International Organization for Biological Control (IOBC) 2008 Abstract Invasive species are generally detected in Polynesia from the exact moment of its introduction new ecosystems long after their first arrival, making it into Tahiti to combat the invasive pest Homalodisca difficult to elucidate pathways leading to successful vitripennis. Within 10 months, the parasitoid spread invasion. In this study, the dispersal of a classical quickly from Tahiti to widely separated islands (up to biological control agent, the mymarid egg parasitoid 1,400 km from Tahiti); presumably through the trans- Gonatocerus ashmeadi, was monitored across ten portation of plant material containing parasitized islands in three major island groups in French H. vitripennis eggs. Gonatocerus ashmeadi thus func- tioned as a ‘‘biomarker’’, providing an informal audit of the effectiveness of inter-island quarantine mea- Handling Editor: Dirk Babendreier. sures designed to curb the accidental spread of noxious J. N. Petit Á J. Grandgirard Á N. Davies organisms. Survey results suggest that invasive orga- Richard B. Gump South Pacific Research Station, nisms, like deliberately released biological control University of California, Berkeley, BP 244, 98728 agents, can be unintentionally and rapidly transmitted Moorea, French Polynesia e-mail: [email protected] across vast distances by humans. Furthermore, even remote islands appear to experience relentless pressure J. Grandgirard from invasive propagules associated with human e-mail: [email protected] travel. Implications of survey work documenting the N. Davies spread and impact of G. ashmeadi are discussed within e-mail: [email protected] the context of biological control programs, non-target impacts, and biosecurity initiatives. M. S. Hoddle (&) Department of Entomology, University of California, Riverside, CA 92521, USA Keywords Biological invasion Á Biosecurity Á e-mail: [email protected] Human-mediated dispersal Á Homalodisca vitripennis Á Invasion pathways Á Quarantine Á M. S. Hoddle Stratified dispersal Center for Invasion Biology, University of California, Riverside, CA 92521, USA G. K. Roderick Introduction Environmental Science, Policy and Management, Division of Insect Biology, University of California, Berkeley, CA 94720, USA Despite the critical role natural dispersal plays in e-mail: [email protected] biological control programs, there is relatively little 123 J. N. Petit et al. information on the dispersal characteristics of natural longevity of *12 days (at 25°C) (Pilkington and enemies (Corbett and Rosenheim 1996; Canto Sila Hoddle 2006). After a *12 month risk assessment et al. 2006). Specifically, how introduced species study (Grandgirard et al. 2007), G. ashmeadi was spread through a new geographic range and the cleared for release by the French Polynesian Govern- factors affecting this dispersal are some of the most ment, and 13,786 parasitoids were released at 27 sites important applied problems in invasion ecology on the island of Tahiti between May 2 and October 25 (Elton 1958; Sallam et al. 2001; Leibhold and Tobin 2005. 2007). The ‘‘natural laboratory’’ setting of island Within seven months post-release, pest popula- archipelagos, such as those of French Polynesia, tions on Tahiti were reduced by more than 95% and facilitates the study of fundamental scientific issues parasitism levels of H. vitripennis eggs averaged 80– regarding biological invasions and natural coloniza- 100% (Grandgirard et al. 2008). Such high levels of tion processes (Gillespie and Roderick 2002). To this parasitism in French Polynesia were likely favored by end, the intentional introduction of a parasitoid as a year round temperatures which favored optimal classical biological control agent into an insular reproductive output (Pilkington and Hoddle 2006), natural laboratory provides a unique opportunity to an abundance of flowering plants in urban areas that monitor the spread of a biological control agent, as a could have provided resources that promoted surrogate, for examining the potential spread of an increased longevity and fecundity of female parasi- invasive species in a new ecosystem. Monitoring can toids (Irvin and Hoddle 2007), and a complete absence commence from the exact moment of the introduction of Proconiini sharpshooters in French Polynesia of the natural enemy with precise records of initial meant G. ashmeadi had no alternative host species propagule pressure, introduction frequencies, and for exploitation which ensured an extremely tight release localities being used to examine the invasion linkage between this natural enemy and its intended dynamics of the biological control agent. target, H. vitripennis (Grandgirard et al. 2007). The glassy-winged sharpshooter, Homalodisca vit- As part of the biological control program against ripennis (Germar) [formerly Homalodisca coagulata H. vitripennis in French Polynesia, we hypothesized (Say) (Takiya et al. 2006)] (Hemiptera: Cicadellidae), that the spread of G. ashmeadi on and among islands is an important exotic insect pest in the South Pacific as well as across vastly separated archipelagos would that most likely originated from California (USA) after follow a stratified dispersal process (Hengeveld 1989; H. vitripennis invaded this state in the late 1980s Petit et al. 2008b). Stratified dispersal is a combina- (Sorensen and Gill 1996). Homalodisca vitripennis is tion of: (1) short-distance localized dispersal by the native to the southeast USA and northeast Mexico organism (e.g., flying or walking), and (2) rapid long- (Sorensen and Gill 1996; Triapitsyn and Phillips distance dispersal assisted by abiotic factors (e.g., 2000). This pest invaded French Polynesia in 1999 wind) or biotic factors (e.g., the unintentional human (Secretariat of the Pacific Community 2002), Hawaii transportation of H. vitripennis egg masses infected in 2004 (Hoover 2004), Easter Island in 2005 (Sandra by G. ashmeadi). The insular island system of French Ide personal communication 2005), and the Cook Polynesia makes it very easy to separate short- Islands in 2007 (Maja Poeshco personal communica- distance dispersal across an island from long-distance tion 2007). The arrival of H. vitripennis on the island of movement between islands and archipelagoes. Tahiti and the subsequent problems resulting from this Controlled releases and subsequent monitoring of invasion were discussed by Grandgirard et al. (2006). natural enemies within the context of a biological In 2004, a classical biological control program against control program provides a rare opportunity for the glassy-winged sharpshooter was initiated in rigorous quantitative ecological studies investi- French Polynesia using the highly specific egg para- gating processes underlying deliberately orchestrated sitoid, Gonatocerus ashmeadi Girault (Hymenoptera: invasions. Such evaluations are important because Mymaridae), a solitary endoparasitoid that attacks unintentional introduction of natural enemies to new eggs of Proconiini sharpshooters (Cicadellidae: areas via unregulated movement (e.g., plants bearing Cicadellinae: Proconiini) (Triapitsyn et al. 1998), the infective propagules such as parasitized eggs), may tribe to which H. vitripennis belongs. Gonatocerus pose significant risk to non-target species if non-targets ashmeadi is \2 mm in length and has an average were not previously considered in risk assessment 123 Elucidating long distance invasion pathways for Gonatocerus ashmeadi studies because they inhabited areas outside of the of G. ashmeadi throughout French Polynesia and initial release foci of the biological control program. evaluate the influence of unintentional human trans- Therefore, biological control programs in ‘‘natural portation on the spread of this deliberately released laboratories’’, such as the islands of French Polynesia, upper trophic level organism. and subsequent research on the spread of natural enemies can potentially improve the efficacy of biosecurity procedures to contain the spread of Material and methods invasive species and to enhance the safety of biological control programs. Understanding the long distance The deliberate release of Gonatocerus ashmeadi dispersal capability of natural enemies and the possible in Tahiti role of humans in unintentionally moving natural enemies are important aspects affecting the outcomes Detailed release methods for G. ashmeadi in Tahiti of biological control programs in terms of both impact are described in Grandgirard et al. (2008). Briefly, on the intended target and safety to non-target species G. ashmeadi was first released at two monitoring sites throughout the range of the target pest. on the north of the island of Tahiti: (1) at sea level in Consequently, the long-distance spread of natural Papenoo (17°30025.0100S; 149°27030.4700W), and (2) enemies, such as G. ashmeadi, can serve as at 800 m in Pirae (17°34021.5800S; 149°31026.7900W) ‘‘biomarkers’’ to help identify the invasion pathways (Fig. 1). The Papenoo site was characterized by: (1) of their hosts, in this instance, the pest H. vitripennis. an extremely high host density, with an average of Here we present data on the long-distance