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A Retrospective Analysis of Known and Potential Risks Associated with Exotic Toadxax-Feeding Insects

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A Retrospective Analysis of Known and Potential Risks Associated with Exotic Toadxax-Feeding Insects Biological Control 35 (2005) 276–287 www.elsevier.com/locate/ybcon A retrospective analysis of known and potential risks associated with exotic toadXax-feeding insects Sharlene E. Sing a,¤, Robert K.D. Peterson b, David K. Weaver b, Richard W. Hansen c, George P. Markin a a U.S. Forest Service, Rocky Mountain Research Station, 1648 S. 7th Avenue, Bozeman, MT 59717, USA b Department of Land Resources and Environmental Sciences, Montana State University, Bozeman, MT, USA c USDA-APHIS-PPQ, Center for Plant Health Science and Technology, Ft. Collins, CO, USA Received 27 August 2004; accepted 18 August 2005 Available online 5 October 2005 Abstract To date, eight exotic toadXax-feeding insect species have been accidentally or intentionally introduced to North America. Reports on their establishment and impact have been recorded for more than 60 years. Environmental risks linked to biological control of toadXax were identiWed in terms of host resources and undesirable impacts on the target species through the critical review of this record. Data gaps revealed during this retrospective analysis are addressed through suggestions for future research and associated experimental meth- odologies. Known and potential impacts of toadXax-feeding insects on both invasive toadXax and non-target species are examined. Recent programmatic demands for demonstrated agent eYcacy and stringent host selectivity during the prerelease screening process clearly illustrate that classical biological control of invasive toadXax in North America is progressing beyond the so-called lottery approach. 2005 Elsevier Inc. All rights reserved. Keywords: ToadXax; Biological control; Invasive weeds; Non-target eVects; Environmental risk 1. Introduction icized for their lack of biological relevance (Withers, 1999), thereby failing as adequate indicators of potential agent Prerelease screening that evaluates biocontrol agent per- performance in the release environment (Harris and McE- formance, in terms of both eYcacy and agent behavior voy, 1995). Furthermore, unresolved taxonomic issues (Arnett and Louda, 2002; Heard, 1999; Marohasy, 1998), related to both the candidate agents and their targets have should reduce potential risks associated with the agent led to the approval of ineVective or inappropriate agents when the agent is approved for release (Baars, 2000; Louda, (Crawley, 1989; Myers and Bazely, 2003; Thomas and Wil- 1998; SchaVner, 2001). Problems with the prerelease screen- lis, 1998). Because prerelease screening tests are so narrowly ing process for candidate agents, aside from the emphasis focused on reducing the potential risk of non-target on detecting non-target impacts at the expense of evaluat- impacts, risks associated with an incomplete knowledge of ing eYcacy (Kluge, 2000), arise from a multitude of meth- agent’s potential performance in the treated ecosystem are odological issues that compromise the value of host signiWcantly increased (Howarth, 2000). selectivity testing (Gassmann and Louda, 2001). Experi- Risks associated with the introduction of exotic weed mental methods used in prerelease screening have been crit- biocontrol agents fall under two broad categories: (1) when the agent causes unintended and deleterious impacts to non-target species, and (2) when the agent fails to reduce * Corresponding author. populations of, or causes undesired impacts on, the target E-mail address: [email protected] (S.E. Sing). weed. Non-target impacts stem primarily from taxonomic 1049-9644/$ - see front matter 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2005.08.004 S.E. Sing et al. / Biological Control 35 (2005) 276–287 277 uncertainty with regard to the target weed and the were: a foliar-feeding moth, Calophasia lunula Hufnagel unknown degree of relatedness it shares, in terms of host (Lepidoptera: Noctuidae) (introduced in 1965); two root- acceptance and suitability, with closely related native, inva- boring moths, Eteobalea serratella Treitschke and E. inter- sive or non-native ornamental relatives (van Klinken, mediella Riedl (Lepidoptera: Cosmopterigidae) (1995); a 2000). Apart from the obvious undesired outcome of being root-galling weevil, Rhinusa linariae Panzer (Coleoptera: ineVective, weed biocontrol agents may actually enhance Curculionidae) (1995); and a stem-mining weevil, Mecinus weed Wtness through inadequate herbivory or other ecolog- janthinus Germar (Coleoptera: Curculionidae) (1995) ical activities. Examples of herbivore-associated undesired (DeClerck-Floate and Harris, 2002; Harris, 1984; Harris impacts to weed species targeted for biological control may and Carder, 1971; McClay and Declerck-Floate, 2002). include: tolerance of herbivory (Strauss and Agrawal, Progress in the biological control of exotic toadXax in 1999); compensatory growth responses to herbivory North America has been reported for more than 50 years (Trumble et al., 1993); facilitation of sexual reproduction (Smith, 1956). This record provides an excellent opportu- through pollination (Barthell et al., 2001; Goulson and nity for retrospective analysis as a relevant and informative Derwent, 2004); production of allelopathic exudates in case study for identifying potential risks and beneWts of response to herbivory (Callaway et al., 1999; Thelen et al., biological control (Hopper, 2001; Louda et al., 2003). The 2005); and semiochemical signaling to herbivore natural following evaluation serves Wrst as a review of documented enemies (Paré and Tumlinson, 1999). examples that conWrm existing problems in the prerelease EYcacious biocontrol agent(s) have been successfully screening of toadXax biocontrol agents. In addition, this identiWed, screened, approved, and released against a num- critique examines how new methods of investigation may ber of exotic weed species targeted in long-term classical potentially enhance the prerelease evaluation process by biological control programs (Coombs et al., 2004; Crawley, identifying potential undesired impacts on the target spe- 1989; Mason and Huber, 2002; Story, 1992). Unfortunately, cies. Specialized spatial and ecological statistical methods many agents have been released with little or no documen- are discussed as analyses that could be performed to tation of impact on target weed populations (Crawley, enhance risk/beneWt assessments for situations where there 1989; Kluge, 2000; McEvoy and Coombs, 1999; Syrett is some indication that biocontrol beneWts might be con- et al., 2000). At the same time, examples of non-target founded by ecological risks associated with the introduc- impacts have been widely publicized (Follett and Duan, tion of a candidate agent. 2000; Howarth, 1991; Louda et al., 1997; Pearson and Call- away, 2003; SimberloV and Stiling, 1996; Wajnberg et al., 1.1. Known and potential risks: host resources 2001). The resulting concerns over biological control safety necessitate new and more careful approaches to prerelease 1.1.1. Identity crisis: target weed taxonomic and genotypic testing. Retrospective assessments of weed biological con- uncertainty trol can function as an exercise in accountability by consol- Consensus on the taxonomic designation of invasive, idating and synthesizing all known information on agent exotic toadXaxes has been elusive. Dalmatian toadXax has interactions with target and non-target species, providing a been treated both as a subspecies of broomleaf toadXax, systematic basis for identifying signiWcant data gaps, partic- (Linaria genistifolia (L.) P. Mill.), L. genistifolia (L.) Miller ularly those concerning non-target impacts, and can be use- ssp. dalmatica (L.) Maire & Petitmengin (Chater et al., ful in improving speciWc aspects of future biocontrol 1972), and as a species entity (L. dalmatica (L.) Miller) com- enterprises (Gassmann and Louda, 2001; Hopper, 2001). pletely separate but closely related to L. genistifolia (Davis, Dalmatian toadXax, Linaria dalmatica (L.) Miller, and 1978; Hartl, 1974; Sutton, 1988). Canadian weed biocontrol yellow toadXax, L. vulgaris (Scrophulariaceae), are short- researchers consider these two species so closely related as lived perennial herbs of Eurasian origin (Alex, 1962; Saner to use the common name “broad-leaved Dalmatian toad- et al., 1995; Vujnovic and Wein, 1997). Dalmatian and yel- Xax” to denote L. dalmatica (L.) Mill., and “narrow-leaved low toadXax are widely distributed throughout North Dalmatian toadXax” for L. genistifolia (Harris and DeCl- America. Between the two species, invasive toadXax popu- erck-Floate, 2003). lations occur in all US states except Hawaii (USDA-NRCS, The USDA, NRCS PLANTS database currently lists 2004) and all Canadian provinces (Saner et al., 1995; Vuj- the species Linaria dalmatica (L.) P. Mill. with two subspe- novic and Wein, 1997). Three toadXax-feeding insect spe- cies: spp. dalmatica and spp. macedonica (Griseb.) D.A. Sut- cies are thought to have been adventitiously introduced on ton, as separate from Linaria genistifolia, a species with one horticultural specimens of these weeds: the Xower-feeding variety, var. genistifolia (USDA-NRCS, 2004). Alex (1962) beetle, Brachypterolus pulicarius (L.) (Coleoptera: Kateri- similarly distinguishes two varieties (rather than subspe- dae), and two seed-capsule feeding weevils, Rhinusa (for- cies) of L. dalmatica, var. dalmatica and var. macedonica, merly Gymnetron) antirrhini Paykull, and R. neta Germar through a list of morphological characters. Alex (1962) (Coleoptera: Curculionidae) (Smith, 1959). Classical bio- believed that L. dalmatica
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