C O N S E R V A T I O N I S S U E S ABSTRACT: Purple loosestrife ( L.) is an invasive nonindigenous that negative- ly affects North American wetlands. In 1992, four host-specific herbivores were introduced from • the plant’s native range as biological control agents and are now established in over 30 states and 10 Canadian provinces. Severe defoliation of purple loosestrife by calmariensis L. and G. pusilla Duft. (Coleoptera: Chrysomelidae) selectively reduced purple loosestrife biomass by as much Nontarget Feeding as 95% at many early release sites. At three sites, mass emergence of new generation Galerucella adults resulted in localized, short-term attack on Rosa multiflora Thunb., Potentilla anserina L., and Decodon verticillatus (L.) Elliott. Individuals of the same plant species away from the immediate emergence of Leaf- areas and at other release sites remained undamaged, and we observed neither feeding nor oviposition on the same by overwintered adults. Attack did not persist into the next growing season, and nontarget plants grew and appeared vigorous the following year, while purple loosestrife remained Introduced suppressed. Such “spillover” does not constitute a host shift; beetles are unable to complete develop- ment on these nontarget plants. Spillover effects have been observed in other biocontrol programs and to Control Purple do not affect distribution or abundance of nontarget species. We anticipate that occasional spillover with transient attack on nontarget species may occur at other release sites with high population densities of Loosestrife (Lythrum the Galerucella species. Careful monitoring is the best means to determine long-term impact.

Alimentación no Preferencial de Escarabajos Defoliadores Introducidos para salicaria L.) Controlar la Loosestrife Púrpura (Lythrum salicaria L.) RESUMEN: Lythrum salicaria L. Es una planta invasora alóctona que afecta negativamente los humedales de norte América. En 1992, se introdujeron cuatro insectos herbívoros huéspedes del rango 1 Bernd Blossey nativo de L. salicaria, que ahora están establecidos en 30 estados y diez provincias canadienses. Department of Natural Resources Galerucella calmariensis L. y G. pusilla Duft (Coleoptera: Chrysomelidae) causaron una severa Fernow Hall defoliación de L. salicaria reduciendo su biomasa en casi el 95% en muchos de los lugares de liberación iniciales. En tres sitios, las nuevas generaciones de Galerucella adultos atacaron localmente a Rosa Cornell University multiflora Thunb., Potentilla anserina L., y Decodon verticillatus (L.) Elliott. Individuos de la misma Ithaca, NY 14853 USA especie de planta, lejos de las áreas inmediatas de emergencia y en otros lugares de liberación permanecen sin ser dañados y no hemos observado alimentación ni oviposición en las mismas plantas Richard Casagrande por los adultos que pasaron el invierno. Los ataques no se mantuvieron en la siguiente estación, y las Lisa Tewksbury plantas que no fueron blanco de los ataques crecieron y parecían vigorosas al año siguiente, mientras que L. salicaria se mantuvo disminuida. Tal cambio momentáneo no constituye un cambio de huésped, Department of Plant Sciences los escarabajos no son capaces de completar su desarrollo fuera de sus plantas huéspedes. Efectos de University of Rhode Island cambios temporales han sido observados en otros programas de biocontrol y no afectan la distribución Kingston, RI 02881 USA o abundancia de las plantas que no sean los blancos. Anticipamos que un cambio ocasional con ataques transitorios a las plantas que no eran los objetivos podía ocurrir en otros sitios de liberación con altas Douglas A. Landis densidades de población de las especies de Galerucella. Un monitoreo cuidadoso es la mejor forma de determinar el impacto a largo término. Department of Entomology & Center for Integrated Plant Systems Index terms: biological control, Decodon verticillatus, nonindigenous invasive species, nontarget Michigan State University feeding, wetlands East Lansing, MI 48824-1311 USA

Robert N. Wiedenmann Center for Economic Entomology Illinois Natural History Survey INTRODUCTION cies (Blossey 1999, Brown 1999, Blossey Champaign, IL 61820 USA et al. 2001). Established L. salicaria pop- Invasive nonindigenous plants constitute a ulations persist for decades, are difficult to Donna R. Ellis major threat to rare and endangered spe- control using conventional techniques Department of Plant Science cies (Wilcove et al. 1998) and the manage- (chemical, physical, mechanical), and con- University of Connecticut ment of natural areas (MacDonald et al. tinue to spread into adjacent areas (Thomp- Storrs, CT 06269 USA 1989, Randall 1996). Purple loosestrife son et al. 1987). A classical biological (Lythrum salicaria L.), a Eurasian peren- weed control program was initiated in 1986 • nial herb introduced to North America in (Malecki et al. 1993), and four host-spe- the early 1800s (Thompson et al. 1987), cific insect herbivores were introduced to 1 Corresponding author e-mail: [email protected] can alter biogeochemical and hydrologi- North America (Malecki et al. 1993, Hight cal processes in wetlands (Emery and Per- et al. 1995) in 1992. The selected species Natural Areas Journal 21:368–377 ry 1996, Grout et al. 1997) and threaten were a root-mining weevil, Hylobius trans- rare and endangered plant and spe- versovittatus Goeze; two leaf-feeding bee-

368 Natural Areas Journal Volume 21 (4), 2001 tles, Galerucella calmariensis L. and G. by the decision to introduce biological species to increase (which should benefit pusilla Duft.; and a flower-feeding weevil, control agents for purple loosestrife (Blos- or allow recovery of native food webs). Nanophyes marmoratus Goeze. sey et al. 1994a, b; Blossey and Schroeder Long-term monitoring programs (incor- 1995). Herbicide treatments actually re- porating target pest, control agent, and Biological control, similar to chemical, sulted in a further increase of purple loose- associated plant and animal communities) mechanical, and physical control, may strife due to superior recruitment from the need to be designed to evaluate the full affect nontarget species. Benefits and risks seed bank and accelerated suppression of ecological impact (positive as well as neg- associated with biological control have native species (Skinner et al. 1994). Host- ative) of biological weed control (Blossey recently received much attention due to specificity tests identified two closely re- 1999, Blossey and Skinner 2000). Biolog- actual or suspected nontarget effects lated native North American species, De- ical control agents for purple loosestrife (Howarth 1991, Simberloff and Stiling codon verticillatus (L.) Elliott (swamp have now been released in over 30 states 1996, Louda et al. 1997, McFadyen 1998, loosestrife or waterwillow) and Lythrum and 10 provinces in the United States and Follett and Duan 2000, Pemberton 2000, alatum Pursh. (winged loosestrife), as po- Canada, and a monitoring program was Wajnberg et al. 2001). Risks to nontarget tentially vulnerable to limited attack by established (Blossey and Skinner 2000) to species need to be weighed against the newly emerged Galerucella beetles (Blos- assess changes in abundance of risks of allowing invasive species to re- sey et al. 1994a, b; Blossey and Schroeder and wetland plant communities. At many main unchecked. Recent reviews of non- 1995). However, the taller L. salicaria not release sites, purple loosestrife is declin- target effects in biological weed control only replaces L. alatum where ranges over- ing, but we also have recently observed (note: we did not consider the safety record lap; in areas where both species co-occur, nontarget feeding by Galerucella spp. The and regulations for insect biological con- the presence of L. salicaria reduces polli- purpose of this paper is to discuss the trol) concluded that host-specificity tests nator visitation and seed set of L. alatum implications of nontarget feeding detected are valuable and accurately predict poten- (Brown 1999). Biocontrol agents were at several field sites for the biological con- tial nontarget effects (McFadyen 1998, introduced based on risk assessments that trol program targeting purple loosestrife. Fowler et al. 2000, Pemberton 2000, Gass- concluded that benefits outweighed po- mann and Louda 2001). Nontarget im- tential risks to L. alatum and D. verticilla- Status of Galerucella calmariensis pacts of Rhinocyllus conicus Fröhlich at- tus (Blossey et al. 1994a,b; Blossey and and G. pusilla tacking native North American Cirsium Schroeder 1995). species (Louda et al. 1997), and of Cacto- Initial releases of the two leaf beetles G. blastis cactorum Berg. attacking native Successful weed biocontrol programs can calmariensis and G. pusilla occurred in Opuntia species in Florida (Simberloff and reduce biomass of target plant species to seven states and six provinces (Hight et al. Stiling 1996), are the result of poor deci- very low levels (McEvoy et al. 1991), al- 1995). Demand for these species quickly sion-making processes before 1970 that lowing other previously suppressed plant exceeded their availability and mass-rear- allowed the release of nonspecific herbi- vores (Pemberton 2000, Gassmann and Louda 2001). Contemporary regulations Table 1. Total number of release sites for biological control agents against purple loosestrife (U.S. Department of Agriculture 1999) in 11 states, sites with quantitative monitoring using a standardized protocol, sites that are incorporate measures to avoid similar mis- visited annually by state or university personnel (“Qualitative Monitoring”), release sites under control by collaborators (“Monitoring Uncertain” due to lack of information about takes (Gassmann and Louda 2001). local monitoring efforts), and year of first release.

Host-specificity tests are designed to pre- Release Quantitative Qualitative Monitoring Year of vent introducing species that may have States Sites Monitoring Monitoring Uncertain 1st Release negative impacts on nontarget species, yet these tests can not eliminate nontarget feed- Rhode Island 5 1 3 0 1994 ing entirely (Pemberton 2000). We must Connecticut 21 20 1 0 1996 be concerned with introducing biological New York 166 27 9 130 1992 control agents if their impact on nontarget New Jersey 42 8 34 0 1994 species reduces distribution and abundance Indiana 45 4 41 0 1994 of these nontarget species. Release of weed Michigan 50 28 20 0 1994 biocontrol agents is often permitted (after environmental assessment), even if the Illinois 212 10 120 82 1994 potential for nontarget attack exists, when Wisconsin 480 51 300 139 1994 potential harm caused by the herbivore is Minnesota 560 20 290 250 1992 thought to be significantly less than harm Colorado 3 3 0 0 1994 caused by other control methods or by the Oregon 100 23 50 27 1992 failure to control the target invasive spe- Total 1684 195 868 628 cies. This assessment process is illustrated

Volume 21 (4), 2001 Natural Areas Journal 369 ing procedures are now widely used by sey 1995a-d). Adults overwinter in the leaf 5-year period (E. Holroyd, Bureau of Rec- state and federal agencies, universities, litter; they emerge in early spring, and lamation, Denver, pers. com.; B. Blossey, schools, and private citizens (Blossey and their feeding causes a characteristic “shot- pers. obs.). Hunt 1999, Klepinger 1999). As a result of hole” pattern. Oviposition peaks in late improved rearing abilities, over 5 million May/early June; first instar larvae feed OBSERVATIONS adults of both Galerucella species were within leaf or flower buds; later instars released in more than 30 states and over feed on all aboveground plant parts. Lar- Observations in summer 1999 in Rhode 1600 wetlands nationwide. Although both val feeding strips the photosynthetic tissue Island, Michigan, and Connecticut at sev- species have very similar life histories off individual leaves creating a “window- eral of the permanent monitoring sites (Blossey 1995c), G. calmariensis was eas- pane” (generally leaving the upper epider- found that severe food limitation for new- ier to mass-produce (Blossey and Hunt mis intact). Mature larvae pupate in the ly emerging adults of Galerucella spp. 1999) and is most likely the dominant spe- litter or soil beneath the host plant. At this resulted in heavy, albeit localized, attack cies in many releases. time (mid- to late June in upstate New of Rosa multiflora, Potentilla anserina, York) the damage to purple loosestrife and Decodon verticillatus (plant nomen- We developed a standardized monitoring becomes most conspicuous. Both Galeru- clature follows Gleason and Cronquist protocol, using permanent quadrats, to cella species are usually univoltine (one 1991). assess the impact of these biocontrol agents generation a year) although a partial sec- on purple loosestrife and the associated ond generation sometimes occurs. Peak Rhode Island plant communities (instructions and forms dispersal of overwintered beetles occurs are available at: www.invasiveplants.net). in spring; new generation beetles have dis- Monitoring is conducted in early summer persal flights shortly after emergence, are The Rhode Island site is located along the during peak insect abundance and at the able to locate host plant patches as far wetland walk at the Roger Williams Park end of the growing season. In addition to away as 1 km within a few days, and are Zoo in Providence. The entire wetland area insect abundance (using time-constrained attracted to conspecifics (Grevstad and is approximately 5.4 ha, half of which is counts), impact on the host plant (leaf area Herzig 1997). covered by purple loosestrife. Zoo records removed), percent cover, height, number indicate attempts to eradicate L. salicaria of stems of purple loosestrife, and pres- Increasingly, observations and quantita- as early as 1984. Other associated wetland ence and abundance of other associated tive data from field releases show that the plants at the site include pussy willow plants are recorded. Table 1 summarizes Galerucella species are able to build up (Salix discolor), black willow (Salix ni- information on the number of release sites large populations with dramatic impacts gra) black tupelo (Nyssa sylvatica), bay- in 11 states. Biocontrol agents were re- on purple loosestrife growth and abun- berry (Myrica pensylvanica), pokeberry leased in 1684 wetlands invaded by purple dance (Blossey and Skinner 2000, (Phytolacca americana), winterberry (Ilex loosestrife. Of these, 195 (11.6%) are mon- Lindgren 2000). Densities of over 8000 verticillata), elderberry (Sambucus sp.), itored using quantitative data collections, eggs m-2 were observed in Manitoba goldenrod (Solidago sp.), Viburnum sp., and 868 (51.5%) are visited at regular in- (Lindgren 2000). In Europe, larval densi- silky dogwood (Cornus amomum), arrow tervals (mostly annually) to collect quali- ties of over 400/stem were common, re- arum (Peltandra virginica), maple (Acer tative data (observations on presence/ab- sulting in complete defoliation of purple sp.), swamp azalea (Rhododendron visco- sence of biocontrol agents, assessment of loosestrife (Blossey 1995b). In North sum), steeplebush (Spiraea tomentosa), population status and impact on purple America, areas dominated by purple loose- swamp willow (Decodon verticillatus), and loosestrife, and potential nontarget effects). strife can have densities >50 stems m-2 Joe-Pye-weed (Eupatorium sp.). All states with active rearing programs (Blossey and Skinner 2000). A conserva- rely on cooperation by local collaborators. tive estimate of 20 purple loosestrife stems A mix of G. calmariensis and G. pusilla We have included these sites in the num- m-2, with 200 larvae/shoot, results in pop- adults (500 in 1994, 600 in 1995, and ber of total release sites but due to uncer- ulations of 4000 larvae m-2; and allowing 3000 in 1996) from Guelph University tainty about monitoring efforts they are for 50% mortality from to adult, an (Ontario, Canada), Cornell University, and placed into the “uncertain” category. emergence of 2000 adults m-2 can be ex- Mission, Texas, were released at the zoo. pected. Using these figures, we can as- In 1994 the first adults were released into The introduction of G. calmariensis and sume that in extensive purple loosestrife a cage that was removed the following G. pusilla has increased the number of populations, a single hectare can produce spring, before adult emergence. Subse- North American Galerucella species to five as many as 20 million new adults. The quent open releases were made in June. (Manguin et al. 1993). All species feed on results of these population explosions are The site has been regularly monitored at wetland plants that may co-occur with widespread defoliations of purple loos- least twice per year for insects and plant purple loosestrife and are easily confused. estrife, causing declines to less than 5% of growth. Establishment of a Galerucella Galerucella calmariensis and G. pusilla its original abundance (Cornell University population was confirmed in 1996 and look alike, share similar life histories, and 1996, Blossey and Skinner 2000). Such 1997, and feeding caused some visible occupy the same ecological niche (Blos- impacts can extend well over 100 ha in a damage to purple loosestrife, with the first

370 Natural Areas Journal Volume 21 (4), 2001 extensive defoliation occurring in June emerged) adults were present, but no eggs defoliated purple loosestrife plants 1998. A limited amount of adult feeding or larvae were found in sample quadrats. throughout the entire study area by late was observed on D. verticillatus, but no All L. salicaria plants in the permanent May. Emergence of the new generation larval development. As part of routine quadrats were heavily defoliated and 100% began in mid-June with many L. salicaria wetland management, park staff mowed desiccated. Insects had spread approxi- plants around the lake showing an abun- all D. verticillatus plants in spring 1999. mately 800 m from the original release dance of adults and extensive feeding dam- Purple loosestrife plants were damaged site, and an estimated 4–6 ha of L. salicar- age. but not defoliated in July 1999, at the time ia were 80–100% defoliated in 1999. when F1 generation adults emerged from University facilities personnel periodical- the soil. However, many of these adults No live purple loosestrife foliage remained ly mow all vegetation, including L. sali- laid eggs, producing a very large second in the emergence area, and beetles were caria, along the lake perimeter outside the generation that defoliated the entire pur- seen resting and dispersing from the site. Galerucella biological control study area. ple loosestrife population in the 5.4-ha Silverweed (Potentilla anserina) plants Although the study area was marked off wetland. Emerging F2 generation adults growing in the middle of a dike-top gravel and was not affected, after vegetation was skeletonized R. multiflora bushes growing road running through the site were ca. cut on 25 June 1999 few L. salicaria plants along the wetland boardwalk in the vicin- 60% defoliated by Galerucella feeding with green tissue remained at the lake. ity of the mass emergence. In addition, we over a distance of about 10 m. Individuals New generation adults that emerged in noticed a single skeletonized new shoot of of P. anserina growing a few meters away June had virtually no L. salicaria to feed S. discolor and one leaf of M. pensylvan- among other plants on the sides of the dike on, and there were no other wetlands with ica with Galerucella feeding. An assess- were untouched. Reference specimens purple loosestrife in the vicinity. Many of ment of the extent of nontarget feeding on collected from P. anserina were unfortu- the F1 adults moved onto two small patch- 20 September 1999 found feeding damage nately lost prior to identification. The na- es of D. verticillatus growing near the study on multiflora rose bushes growing as far tive leaf- G. quebecensis Brown is site. Before plants were cut, Galerucella away as 50 m, but no damage on those 100 known to feed on Potentilla spp., therefore adults were not observed feeding on Dec- m away. Other wetland plants in the vicin- there is the possibility that the insects at- odon. Within several days, the D. verticil- ity did not show any signs of attack. All tacking P. anserina were actually G. que- latus plants were completely defoliated. reference specimens collected from R. becensis. However, the similarity to the Small groups of L. salicaria seedlings re- multiflora, S. discolor, and M. pensylvan- situation in Rhode Island and Connecticut grew during the remainder of the summer, ica were identified as G. calmariensis. leads us to interpret these observations as and Galerucella feeding and recruitment a likely case of nontarget feeding. were observed on these plants, whereas D. verticillatus did not regrow in 1999. At a Michigan second release site in Connecticut with a Connecticut The Michigan release site was the Nayan- mix of L. salicaria and D. verticillatus, quing Point Wildlife Area, Bay County, an At the Connecticut site, purple loosestrife Galerucella spp. are established and the impounded Saginaw Bay coastal wetland grows in a narrow fringe around a 2-ha population is increasing, but feeding and managed as a wildlife refuge and hunting lake located in the center of the University oviposition is restricted to purple loose- area, where purple loosestrife infests 40.5 of Connecticut campus in Storrs. Associ- strife. ha and dominates 4.5 ha. Associated wet- ated wetland plants include D. verticilla- land plants include bluejoint (Calamagros- tus, sedges (Carex spp.), jewelweed (Im- Other Sites and Summary tis canadensis), rush (Juncus sp.), hearts- patiens capensis), rice cut-grass, yellow ease (Polygonum lapathifolium), iris (Iris pseudacorus), goldenrod, North- At the Amwell Lake Wildlife Management spike-rush (Eleocharis sp.), and rice-cut ern bugleweed (Lycopus uniflorus), arrow- Area in Hunterdon County, New Jersey, grass (Leersia oryzoides). A mixture of leaved tearthumb (Polygonum sagittatum) newly emerged Galerucella spp. adults fed approximately 500 G. calmariensis and G. asters (Aster spp.), and dodder (Cuscuta on R. multiflora during a population ex- pusilla originating from Cornell Universi- sp.). A mix of 1000 adults of G. calmarien- plosion in summer 2000 (M. Mayer and R. ty were released in sleeve cages in July sis and G. pusilla obtained from Cornell Chianese, New Jersey Department of Ag- 1994. Monitoring was conducted weekly University were released on 2 July 1996. riculture, Trenton, pers. com.). Adult feed- from 19 June–2 August 1995 to evaluate Beetle establishment and impact were mon- ing was restricted to foliage of R. multiflo- establishment (Dalgarn and Kantak 1995). itored using the standardized monitoring ra within a 1-m area adjacent to defoliated The site was visited in 1997 and 1998 to protocol and permanent quadrats along a purple loosestrife, and no larvae or eggs confirm continued insect activity. Moder- 45-m linear transect. Leaf-beetles became were observed. At all other monitoring ate defoliation of L. salicaria was observed established and extensive damage to pur- sites across North America (Table 1), de- in 1998 in a limited area near the release ple loosestrife was obvious in the summer spite similar population explosions of the site. The site was surveyed on 29 June of 1998. In spring 1999, Galerucella adults Galerucella spp., no nontarget feeding was 1999 using procedures of the standardized and eggs were abundant around the entire ever observed. It is critical to confirm spe- monitoring protocol. Teneral (newly lake perimeter; larval feeding completely cies identification of Galerucella spp. Sev-

Volume 21 (4), 2001 Natural Areas Journal 371 eral initially suspected nontarget attacks agents may attack nontarget plants and (2) jecting suboptimal plants that often elicit in Minnesota were found to be the feeding biocontrol agents may, over evolutionary deleterious postingestive effects (Bernays by other native chrysomelid species such time, become less host-specific and attack 1998). Under severe food limitation newly as the waterlily Galerucella nontarget species (Secord and Kareiva emerged adults appear to make “mistakes” nymphaeae (L.), (L. Skinner, Minnesota 1996, Simberloff and Stiling 1996, Louda in their food choice. That such feeding is Department of Natural Resources, St. Paul, et al. 1997). Worldwide, more than 1200 spatially limited to plants (or branches) pers. com.). programs have released 350 species of close to mass emergence sites suggests insects and pathogens targeting 133 plant that adults quickly learn to recognize un- At the three sites with nontarget feeding in species (Julien and Griffiths 1998). Sever- suitable species and leave the area in search 1999, attacked or defoliated plant individ- al recent analyses (McFadyen 1998, Fowl- of suitable host plants. uals re-grew in 2000 and appeared healthy. er et al. 2000, Pemberton 2000) concluded Leaf beetle populations were much lower, that host ranges of herbivorous biological Host-specificity screening results for the but purple loosestrife growth was greatly control agents appear stable, and that non- two Galerucella species in Europe (Blos- suppressed. At Nayanquing in Michigan, target use (defined as the ability to com- sey et al. 1994a, b) led to predictions that cover of purple loosestrife dropped from plete larval development) is largely re- temporary attack on D. verticillatus and L. over 39.8% to 3.2%, and native wetland stricted to close relatives (usually within alatum was likely, particularly at high den- plants have greatly expanded in frequency the same genus) of the target weed species sities of the control agents. These predic- and cover (D. Landis, unpubl. data). Con- (often predicted by host-specificity tests). tions were confirmed and, as predicted, tinued observations of P. anserina plants Although 24 (6.8 %) of all insect biocon- attack was temporary and of no lasting attacked in 1999 showed that no individu- trol agents are reported feeding on nontar- consequence to D. verticillatus and L. ala- al received more than a trace of feeding get plants (Table 2), 10 of these instances tum in Ontario (Corrigan et al. 1998). Our (<1% leaf area removed) in 2000. Howev- can be classified as “spillover” and do not observations in Connecticut and Rhode er, at an adjacent area with complete defo- constitute host shifts. These herbivores are Island further confirm these results. Addi- liation of purple loosestrife in 2000, G. unable to complete development on the tional host-specificity testing of G. cal- calmariensis teneral adults attacked sever- nontarget species and feeding instances mariensis using 40 previously untested al branches of Cornus stolonifera L. At the are associated with population outbreaks. species supported the pre-introduction sites in Connecticut and Rhode Island, no Interestingly, which plant species will be host-specificity results (Kaufman and Lan- nontarget feeding was observed on plants attacked during spillover events seems to dis 2000). Although in no-choice feeding that adults had fed on in 1999 (note that be unpredictable (Table 2). Of larger con- trials adult G. calmariensis nibbled on other these beetles are the same individuals that cern are weed biocontrol agents that es- species, particularly rosaceous plants, nor- fed on nontarget plants as teneral adults!). tablish and sustain populations on nontar- mal feeding, oviposition, and larval devel- This supports data from host-specificity get plants. In many instances survival and opment was restricted to L. salicaria (Kauf- screening indicating that overwintered recruitment is low (Turner 1985, Willis man and Landis 2000). Over 1600 release adults are more selective than inexperi- and Ash 1996) and attack of the nontarget sites are now established throughout North enced, newly emerged beetles (Blossey et is reduced as distance to the original host America (many with sharply increasing al. 1994b). Feeding declined sharply with increases (A. Willis, CSIRO, Canberra, Galerucella populations 4–5 years after increasing distance from the emergence Australia, pers. com.; S. Schooler, Oregon the initial release). Nontarget feeding is area, consistent with the expectations that State University, Corvallis, Oregon, pers. restricted to observations in Ontario (Cor- inexperienced newly emerged adults learn com.). Only 4 (1.7%) species are known to rigan et al. 1998) and those reported in this to avoid unsuitable host plants (Bernays have established self-sustaining popula- paper. The limited duration and extent of 1998). Pheromones of the Galerucella tions on nontarget species in the absence this attack does not affect distribution or species may contribute to the very local- of the original host (Table 2), and this abundance of the nontarget species. ized (a branch or a leaf) attack reported: potential was known at the time of intro- adults are attracted to each other (Grevs- duction. Host-specificity screening con- The benefits of biological control must tad and Herzig 1997) and show highly sistently has provided the best assurance continue to be weighed against the risks of aggregated distributions (Blossey 1995c). for the safety of nontarget species (Mc- nontarget attack, risks of allowing inva- Such “spillover” nontarget effects are lo- Fadyen 1998, Pemberton 2000, Gassmann sive species to remain unchecked, and risks calized, temporary, and restricted to pop- and Louda 2001). associated with other control measures ulation outbreaks of biological control (Blossey et al. 2001). We believe that de- agents. Spillover events, as described here for the spite the very limited incidence of nontar- Galerucella species and other biocontrol get feeding reported in this paper, the re- agents (Table 2), are associated with high lease of biocontrol agents against purple DISCUSSION population densities of control agents, of- loosestrife will have a very positive effect Release of insect herbivores from the home ten newly emerging adults, and food short- on North American wetland ecosystems. range of a nonindigenous plant is often age. These individuals have to learn to At many biocontrol release sites, once- met with concerns that (1) biocontrol recognize suitable host plants while re- monotypic stands of L. salicaria are being

372 Natural Areas Journal Volume 21 (4), 2001 Dennill et al. 1993 Yes Corrigan et al. 1998 No this paper No No No McEvoy and Coombs 2000 Pemberton 2000 Louda et al. 1997 Pemberton 2000 Expected/ No Dennill et al. 1999 Predicted Reference Yes McFadyen 1998 NoYes McFadyen 1998 Blossey et al. 1994a Yes Diehl and McEvoy 1990 (DC) No Pemberton 2000 attack nontarget plants at high population densities but do not he absence of the original host; and “unclassified” species are spp. Yes Turner et al. 1987 L. No Davies and Greathead 1967 species Yes Simberloff and Stiling 1996 spp., pickerel weed No Harris 1988 anserina Cirsium

Opuntia spp. No1982 Center Canna Pontederia Sesamum indicum Acacia melanoxylon Paraserianthes lophanta Nontargets Attacked Myoporum sandwichense Gray Rubus hawaiiensis Decodon verticillatus Helianthus annuus Rosa multiflora Salix discolor Potentilla Cornus stolinifera Senecio triangularis Senecio integerrimus Senecio pseudaureus USA 1972 Released Hawaii 1902 Hawaii 1961Australia 1966 Basil and other herbs No McFadyen 1998 L.1984 India (L.) (L.) Australia 1922 Australia 1922 Melons, tomatoes melons, tomatoes, nectarines, No No 1988 Harris (L.) Caribbean 1957 Native L. New Zealand 1929 L. USA, Canada 1992 (Andrews) South Africa 1982 L. USA 1969native 22 L. Uganda 1960 Link Hawaii 1964 Eichornia crassipes (Martius) Solms-Laubach water hyacinth Opuntia ficus-indica prickly pear Opuntia ficus-indica prickly pear dates, peaches, and grapes Target Weed lantana Lantana camara Willdenow, long leaved wattle Lantana camara Rubus argutus prickly Florida blackberry Parthenium hysterophorus parthenium Lythrum salicaria Senecio jacobaea ragwort USA 1959 Carduus nutans nodding thistle prickly pear in Florida Pemberton 1995 L. Pallister (Warner) (Stal) (Berg) Clarke (Froehlich) Duft. purple loosestrife (Burmeister) L. Pic develop on these species; “sustained attack” species are those that able to sustain populations the nontarget plant in t Table 2. Biological weed control agents and their attack on damage to nontarget plants. “Spillover” species are those that those for which there is insufficient information to place them in either category. SPILLOVER Neochetina eichhorniae Cactoblastus cactorum Chelnidae tabulata Trichilogaster acaciaelongifoliaelongifolia Acacia Agent Teleonemia scrupulosa (Froggatt) Uroplata girardi Croesia zimmermannii Zygogramma bicolorata Galerucella pusilla Galerucella calmariensis SUSTAINED ATTACK Tyria jacobaeae Rhinocyllus conicus Cactoblastus cactorumficus-indica Opuntia

Volume 21 (4), 2001 Natural Areas Journal 373 Lincoln, New Zealand, pers.com. Cullen 1990 Cullen 1990 A. Willis, CSIRO, Canberra, Australia, pers.com. No P. Syrett, Landcare Research, ? Pemberton 2000 ? Pemberton 2000 ? Pemberton 2000 Yes Willis and Ash 1996; Expected/ Predicted Reference ? Julien and Griffiths 1998 ? Pemberton 2000 Torr. ?1985 Turner (L.) ? Turner 1985 Benth. Andres 1985 Benth. Benth. ? ? Turner 1985 Turner 1985 L. Yes Ehler 1991 and 2 other ? Turner 1985 spp.2000 Pemberton calycinum Chamaecytisus palmensis Rubus hawaiiensis Rubus macraei Philoxerus vermicularis R.Br. Alternanthera flavescens Rubus hawaiiensis Rubus macraei Hypericum concinnum Hypericum concinnum Kallstroemia grandiflora K. grandiflora Kallstroemia Nontargets Attacked Clidemia hirta Cyperus polystachyos USA 1971 Released Hawaii 1902 Hawaii 1925 L.1946 USA L.1950 USA L. L.1950 USA Australia 1991 L. USA 1961 L. USA 1961 (L) Link1987 Zealand New Link Hawaii 1963 Link Hawaii 1966 Alternanthera phylloxeroides St. John’s wort, Klamath weed Cytisus scoparius broom Rubus argutus prickly Florida blackberry (Mart.) Griseb. alligatorweed Hypericum perforatum Hypericum perforatum Hypericum perforatum Rubus argutus prickly Florida blackberry Target Weed puncturevine Tribulus terrestris Lantana. camara Cyperus rotundus purple nut-sedge Hübner (Suffr.) Pastrana Kieffer Fabricius Marshall (Lepeletier) (Creutzer) Liro (Druce) (Wollaston) Val) continued Table 2, Chrysolina quadrigemina UNCLASSIFIED Bruchidius villosus Arcola (Vogtia) malloi Priophorus morio Schreckensteinia festaliella hyperici Zeuxidiplosis giardi Aculus hyperici (Jacquelin du Tmolus echion Microlarinus lareyniiterrestris Tribulus Agent M. lypriformis Athesapeuta cyperi

374 Natural Areas Journal Volume 21 (4), 2001 replaced by more diverse wetland plant Lynch, eds., Biological Control: Benefits Bernd Blossey is Assistant Professor and and Risks. Cambridge University Press, communities (D. Landis, R. Wiedenmann, Director of the Biological Control of Non- unpubl. data). At the Tonawanda Wildlife Cambridge, U.K. Indigenous Plant Species Program at Cor- Blossey, B. 1995b. Impact of Galerucella pu- Management Area in western New York nell University. He is developing biologi- State, an area once dominated by purple silla Duft. and G. calmariensis L. (Co- cal control programs for invasive plants in leoptera: Chrysomelidae) on field popula- loosestrife and abandoned by black terns natural areas and is interested in changes tions of purple loosestrife (Lythrum salicaria (Chlidonias niger [L.]) has developed into in native fauna and flora associated with L.). Pp. 27-32 in E.S. Delfosse and R.R. an emergent marsh and is now again used invasion and decline of nonindigenous Scott, eds., Proceedings of the VIII Interna- as a breeding and foraging area for terns plants. tional Symposium on the Biological Con- (D. Carroll, New York Department of En- trol of Weeds, 2–7 February 1992, Canter- bury, New Zealand. DSIR/CSIRO, vironmental Conservation, Alabama, N.Y., Richard Casagrande is Professor of Ento- pers. com.; B. Blossey, pers. obs.). In a Melbourne, Australia. mology at the University of Rhode Island Blossey, B. 1995c. Coexistence of two com- near-monotypic stand of purple loosestrife where his research interests focus on bio- in a highly disturbed wetland in north- petitors in the same fundamental niche: dis- logical control of insects and weeds. tribution, adult phenology and oviposition. western Illinois, 17 native plant species Oikos 74:225-234. not previously observed were recorded in Lisa Tewksbury is Research Associate at Blossey, B. 1995d. A comparison of various 1999 after extensive defoliation by the the University of Rhode Island, specializ- approaches for evaluating potential biolog- Galerucella species (R. Wiedenmann, un- ing in biological control of insects and ical control agents using insects on Lythrum publ. data). Similar results are expected to weeds. salicaria. Biological Control 5:113-122. occur throughout the country, and we will Blossey, B. 1999. Before, during, and after: the continue our long-term monitoring pro- Doug Landis is a Professor in the Depart- need for long-term monitoring in invasive gram to assess changes associated with the ment of Entomology and Associate Direc- plant species management. Biological In- vasions 1:301-311. release of biological control agents for tor of the Center for Integrated Plant Sys- purple loosestrife. tems at Michigan State University. His Blossey, B. 2001. Biological control of an in- vasive wetland plant: monitoring the im- research interests are in insect ecology pact of beetles introduced to control purple The history of biological weed control and and biological control using . current information suggest that nontarget loosestrife. Pp. 451-464 in R.B. Rader, D.P. Batzer, and S. Wissinger, eds., Biomonitor- feeding events are transient, only occur in Robert Wiedenmann is the Director of the ing and Management of North American years of extremely high Galerucella pop- Center for Economic Entomology, Illinois Freshwater Wetlands. John Wiley and Sons, ulations, and are spatially limited to plants Natural History Survey, where he leads New York. close to high emergence areas. Short-term, research and outreach on biological con- Blossey, B. and T. Hunt. 1999. Mass rearing transient, nontarget effects of biological trol of invasive insect and weed pests. methods for Galerucella calmariensis and control agents are acceptable if the net G. pusilla (Coleoptera: Chrysomelidae), biological control agents of Lythrum sali- effect is a benefit to native taxa and eco- Donna Ellis is Associate Extension Edu- systems. caria (Lythraceae). Journal of Economic cator in the Department of Plant Science Entomology 92:325-334. at the University of Connecticut. She con- Blossey, B. and D. Schroeder. 1995. Host spec- ducts applied research and outreach edu- ificity of three potential biological weed ACKNOWLEDGMENTS cational programs for biological control control agents attacking flowers and seeds projects, including invasive plant species. of Lythrum salicaria (purple loosestrife). Thanks to T. Willis and P. Syrett for shar- Biological Control 5:47-53. ing some unpublished information on non- Blossey, B. and L. Skinner. 2000. Design and target effects of biocontrol agents in Aus- LITERATURE CITED importance of post release monitoring. Pp. tralia and New Zealand. V. Nuzzo and Andres, L.A. 1985. Interaction of Chrysolina 693-706 in N.R. Spencer, ed., Proceedings several anonymous reviewers commented quadrigemina and Hypericum spp. in Cali- of the X International Symposium on Bio- on earlier versions of this paper. L. Skin- fornia. Pp. 235-239 in E.S. Delfosse, ed., logical Control of Weeds, 4–10 July 1999, ner, Minnesota Department of Natural Proceedings of the VI International Sympo- Montana State University, Bozeman. Resources; R. Dunbar, Indiana Department sium on Biological Control of Weeds, 19– Blossey, B., D. Schroeder, S.D. Hight, and of Natural Resources; M. Mayer and R. 25 August 1984. Agriculture Canada, R.A. Malecki. 1994a. Host specificity and Chianese, New Jersey Department of Ag- Ottawa. environmental impact of the weevil Hylo- bius transversovittatus, a biological control riculture; E. Coombs, Oregon Department Bernays, E.A. 1998. Evolution of feeding be- agent of purple loosestrife (Lythrum sali- of Agriculture; S. Schooler, Oregon State havior in insect herbivores. BioScience 48:35-44. caria). Weed Science 42:128-133. University; B. Woods, Wisconsin Depart- Blossey, B., D. Schroeder, S.D. Hight, and ment of Natural Resources; and D. Eberts Blossey, B. 1995a. Host specificity screening of insect biological weed control agents as R.A. Malecki. 1994b. Host specificity and and E. Holroyd, Bureau of Reclamation, part of an environmental risk assessment. environmental impact of two leaf beetles Denver, provided information on monitor- Pp. 84-89 in H.M.T. Hokkanen and J.M. (Galerucella calmariensis and G. pusilla) ing efforts. for the biological control of purple loose-

Volume 21 (4), 2001 Natural Areas Journal 375 strife (Lythrum salicaria). Weed Science on Biological Control of Weeds, 6–11 specificity testing of Galerucella calmarien- 42:134-140. March 1988. Ministero dell’ Agricola e delle sis L. (Coleoptera: Chrysomelidae) on wild Blossey, B., L.C. Skinner, and J. Taylor. 2001. Foreste, Rome, and CSIRO, Melbourne, and ornamental plant species. Biological Impact and management of purple loose- Australia. Control 18:157-164. strife (Lythrum salicaria) in North Ameri- Ehler, L.E. 1991. Planned introduction in bio- Klepinger, M. 1999. The Purple Loosestrife ca. and Conservation 10:1787- logical control. Pp. 21-39 in L. Ginzburg, Project cooperators handbook. Extension 1807. ed., Assessing Ecological Risks of Biotech- Bulletin E-2690 sections 1-4, Michigan State Brown, B. 1999. The impact of an invasive nology. Butterworth-Heineman, Boston, University, East Lansing. 276 pp. species (Lythrum salicaria) on pollination Mass. Lindgren, C.J. 2000. 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Department of demic Publishers, Norwell, Mass. 316 pp. Natural Resources, Ithaca, N.Y. 4 pp. Fowler, S.A., P. Syrett, and R.L. Hill. 2000. Louda, S.M., D. Kendall, J. Connor, and D. Simberloff. 1997. Ecological effects of an Corrigan, J.E., D.L. MacKenzie, and L. Sims- Success and safety in the biological control of environmental weeds in New Zealand. insect introduced for the biological control er. 1998. Field observations of nontarget of weeds. Science 277:1088-1090. feeding by Galerucella calmariensis (Co- Australian Journal of Ecology 25:553-562. leoptera: Chrysomelidae), an introduced Gassmann, A. and S.M. Louda. 2001. Rhi- MacDonald, I.A., L.L. Loope, M.B. Usher, biological control agent of purple loosestrife, nocyllus conicus: initial evaluation and sub- and O. Hamann. 1989. Wildlife conserva- Lythrum salicaria (Lythraceae). Proceed- sequent ecological impacts in North Amer- tion and the invasion of nature reserves by ings of the Entomological Society of Ontar- ica. Pp. 147-183 in E. Wajnberg, J.K. Scott, introduced species: a global perspective. io 129:99-106. and P.C. Quimby, eds., Evaluating Indirect Pp. 215-255 in Drake, J.A., H.A. Mooney, F. di Castri, R.H. Groves, F.J. Kruger, M. Cullen, J.M. 1990. Current problems in host Ecological Effects of Biological Control. Rejmanék, and M. Williamson, eds., Bio- in CABI Publishing, Wallingford, U.K. specificity screening. Pp. 27-36 E.S. logical Invasion: A Global Perspective. John Delfosse, ed., Proceedings VII Internation- Gleason, H.A. and A. Cronquist. 1991. Manual Wiley and Sons, Chichester, U.K. al Symposium on Biological Control of of Vascular Plants of Northeastern United Weeds, 6–11 March 1988. Ministero dell’ States and Adjacent Canada. The New York Malecki, R.A., B. Blossey, S.D. Hight, D. Agricola e delle Foreste, Rome, and CSIRO, Botanical Garden, New York. 910 pp. Schroeder, L.T. Kok, and J.R. Coulson. 1993. Biological control of purple loose- Melbourne, Australia. Grevstad, F.S. and A.L. Herzig. 1997. Quanti- strife. BioScience 43:480-486. Dalgarn, D. and G. Kantak. 1995. Monitoring fying the effects of distance and conspecif- Galerucella spp. release sites for control of ics on colonization: experiments and mod- Manguin, S., R. White, B. Blossey, and S.D. purple loosestrife. 1995 final report to the els using the loosestrife leaf beetle, Hight. 1993. Genetics, , and ecol- Michigan Department of Natural Resources, Galerucella calmariensis. Oecologia ogy of certain species of Galerucella (Co- Wildlife Division, Lansing. 20 pp. 110:60-68. leoptera: Chrysomelidae). Annals of the Entomological Society of America 86:397- Davies, J.C. and D.J. Greathead. 1967. Occur- Grout, J.A., C.D. Levings, and J.S. Richard- 410. rence of Teleonemia scrupulosa on Sesam- son. 1997. Decomposition rates of purple um indicum Linn. in Uganda. Nature loosestrife (Lythrum salicaria) and Lyng- McEvoy, P.B. and E.M. Coombs. 2000. 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376 Natural Areas Journal Volume 21 (4), 2001 Randall, J.M. 1996. Weed control for the pres- Turner, C.E. 1985. Conflicting interests and Wajnberg, E., J.K. Scott, and P.C. Quimby ervation of biological diversity. Weed Tech- biological control of weeds. Pp. 203-224 in (eds.). 2001. Evaluating Indirect Ecologi- nology 10:370-383. E.S. Delfosse, ed., Proceedings of the VI cal Effects of Biological Control. CABI Secord, D. and P. Kareiva. 1996. Perils and International Symposium on Biological Publishing, Wallingford, U.K. 261 pp. pitfalls in the host specificity paradigm. Control of Weeds, 19–25 August 1984, Wilcove, D.S., D. Rothstein, J. Dubow, A. BioScience 46:448-453. Agriculture Canada, Ottawa. Phillips, and E. Losos. 1998. Quantifying Simberloff, D. and P. Stiling. 1996. How risky Turner, C.E., R.W. Pemberton, and S.S. threats to imperiled species in the United is biological control? Ecology 77:1965- Rosenthal. 1987. Host utilization of native States. BioScience 48:607-615. 1974. Cirsium thistles (Asteraceae) by the intro- Willis, A.J. and J.E. Ash. 1996. Combinations duced weevil Rhinocyllus conicus (Co- of stress and herbivory by a biological con- Skinner, L.C., W.C. Rendall, and E.L. Fuge. leoptera: Curculionidae) in California. En- 1994. Minnesota’s Purple Loosestrife Pro- trol mite on the growth of target and nontar- vironmental Entomology 16:111-115. gram: history, findings and management get native species of Hypericum in Austra- recommendations. Special Publication 145, U.S. Department of Agriculture. 1999. Review- lia. Pp. 93-100 in V.C. Moran and J.H. Minnesota Department of Natural Re- er’s manual for the Technical Advisory Hoffmann, eds., Proceedings of the IX In- sources, St. Paul. 27 pp. Group for Biological Control Agents of ternational Symposium on Biological Con- Weeds. U.S. Department of Agriculture, trol of Weeds, 19–26 January 1996, Uni- Thompson, D.Q., R.L. Stuckey, and E.B. Animal and Plant Health Inspection Service versity of Cape Town, Stellenbosch, South Thompson. 1987. Spread, impact, and con- (APHIS), Manuals Unit of Plant Protection Africa. Lythrum salicar- trol of purple loosestrife ( and Quarantine, Frederick, Md. ia) in North American wetlands. Fish and Wildlife Research 2, U.S. Fish and Wildlife Service, Washington, D.C., 55 pp.

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