BioControl DOI 10.1007/s10526-011-9417-z

Status of an ongoing biological control program for the invasive vine, Persicaria perfoliata in eastern North America

J. Hough-Goldstein • E. Lake • R. Reardon

Received: 15 March 2011 / Accepted: 9 October 2011 Ó International Organization for Biological Control (IOBC) 2011

Abstract Mile-a-minute weed, Persicaria perfoliat- human-assisted dispersal of R. latipes is reducing its a (L.) H. Gross (Polygonaceae), an aggressive annual negative effects. Here we review and assess the current vine native to Asia, has invaded forest edges, light status of the biological control program. gaps, open fields, and riparian borders in eastern North America. It was accidentally introduced into Pennsyl- Keywords Weed biocontrol Á Polygonaceae Á vania in the 1930s and has since expanded its range Caryophyllales Á Coleoptera Á Curculionidae north to Massachusetts, south to North Carolina, and west to Ohio. A biological control program was initiated in 1996, and in 2004, a permit was issued for release of Rhinoncomimus latipes Korotyaev (Cole- optera: Curculionidae), a host-specific weevil initially Introduction collected in China. Since 2004, the biology of the weevil in its introduced range has been studied, along Mile-a-minute weed, Persicaria perfoliata (L.) H. with its impact on P. perfoliata, which can be Gross (Polygonaceae; Hinds and Freeman 2005)isan substantial. Weevils have been released in ten states aggressive annual vine native to Asia, which has been through 2010, and populations have increased consid- the subject of a biological control program since 1996. erably at many sites. Although P. perfoliata continues This program is ongoing, as the plant continues to to expand its North American range, natural and spread in the eastern U.S. and the imported biocontrol weevil continues to disperse both on its own and through human effort. Here we review and assess the current status of this program. Persicaria perfoliata has characteristic triangular Handling Editor: Mark Hoddle leaves, flared ocrea (bracts) surrounding the stems, and small backward-projecting spines. Although in Asia it & J. Hough-Goldstein ( ) Á E. Lake is typically found along stream banks (Hyatt and Araki Department of Entomology and Wildlife Ecology, University of Delaware, Newark, DE 19716-2160, USA 2006; Ohwi 1965), in the U.S. it also invades disturbed e-mail: [email protected] open areas and forest edges (Wu et al. 2002). Seeds germinate early in the spring and plants usually R. Reardon emerge in mid-April to early May in the Mid-Atlantic Forest Health Technology Enterprise Team, USDA Forest Service, 180 Canfield St., Morgantown, WV 26505-3101, region of the U.S. (Hough-Goldstein et al. 2008a). USA As suggested by the common name, mile-a-minute 123 J. Hough-Goldstein et al. vines can grow rapidly, and reach lengths of up to 6 m contrasts with the situation in the U.S., where prior to (Mountain 1989). Vines can overtop other plants and introduction of a biocontrol agent, P. perfoliata grew produce masses of intertwining foliage. The impacts nearly free of insect damage. One exception to this is of P. perfoliata include the inhibition of reforestation the Japanese beetle, Popillia japonica L., which and natural forest regeneration by smothering tree occasionally damages the plant during its relatively seedlings, interference with recreational use of natural brief period of adult feeding in mid-summer (personal areas, reduction in quality wildlife habitat, and likely observation; Fredericks 2001). Wheeler and Mengel negative effects on native flora (McCormick and (1984) surveyed the insects feeding on P. perfoliata in Hartwig 1995; Wu et al. 2002). Isolated individual Pennsylvania, and although 40 different species were plants can produce thousands of seeds (achenes) found, none were numerous enough to cause much during the summer and fall (Hough-Goldstein et al. damage. Similar results were found by Fredericks 2008b), which can survive for up to six years in the (2001). This suggests that the ability of mile-a-minute seed bank (Hough-Goldstein et al. 2008a). Many seeds weed to dominate communities in North America is at are shed and germinate under the previous year’s least partially due to the lack of insects damaging the plants, leading to seedling densities averaging as high plant, in comparison to Asia, where the plant’s growth as 200–500 per 0.5 m2 in the introduced range is suppressed by the feeding of numerous insect (Hough-Goldstein et al. 2009). Seeds are also dis- species and where it rarely forms large monocultures. persed by birds, deer, and water (Hough-Goldstein The ‘enemy release hypothesis’ is one explanation et al. 2008a). for why plant species are sometimes able to become Moul (1948) reported that P. perfoliata was first much more dominant in their introduced range than in introduced as a contaminant of holly seed sent from their native range (Joshi and Vrieling 2005; Keane and Japan to a nursery near York, PA, USA ‘‘about Crawley 2002; Maron and Vila 2001), and P. perfo- ten years earlier’’. Before 1980, the plant’s range was liata is probably a good example of enemy release. confined to five counties in Pennsylvania (Hill et al. This was disputed by Hyatt and Araki (2006) who 1981) and six counties in Maryland (Riefner and found that the major source of P. perfoliata mortality Windler 1979). Figure 1 shows the U.S. counties in Japan at their study sites was annual flooding, which reporting presence of mile-a-minute weed over time. did not occur at their U.S. sites. However, the presence This pattern of spread is consistent with Moul’s (1948) of another major mortality factor in the native range report of a single introduction (with establishment) for does not preclude successful biological control in the mile-a-minute weed in the U.S., and subsequent introduced range: if a host-specific herbivore is dispersal attributable to birds, mammals, and water brought to the new range without its own suite of via streams (Riefner 1982). The presence of a ‘‘lag natural enemies and with few competitors for an phase’’ between the time of establishment and that of abundant host plant, it can increase to far higher rapid population growth and spread is typical of populations than are observed in the home range. introductions of invasive plants (Mack et al. 2000; There is also some evidence that mile-a-minute Radosevich et al. 2003), and may simply reflect the weed may have evolved increased competitive ability early phase of exponential population growth, or may and reduced its investment in defense in the absence of result from other factors such as evolutionary change effective herbivores during its first 75 or so years in in the new range (Sakai et al. 2001). Mile-a-minute North America (Guo et al. 2011), a possible example weed is continuing to spread, most recently to of the ‘evolution of increased competitive ability’ Massachusetts to the north (IPANE 2011) and North hypothesis, or EICA (Blossey and No¨tzold 1995). The Carolina to the south (Iverson 2010; Poindexter 2010). EICA hypothesis can also explain invasiveness of A biological control program for mile-a-minute certain plants in their introduced range, and has been weed was initiated by the USDA Forest Service in supported for some invasive plants (e.g. Zou et al. 1996 (Wu et al. 2002). More than 100 insect species 2008) but not for others (e.g. Franks et al. 2008). If true were found feeding on P. perfoliata in China (Ding for P. perfoliata, this makes it even more likely that an et al. 2004), including foliar feeders, stem borers, and introduced host-specific insect could impact the pop- seed and fruit-feeders. The plant typically sustains ulation of invasive mile-a-minute weed in the U.S. heavy feeding damage from insects in China. This North American populations of mile-a-minute were 123 Status of an ongoing biological control program

Fig. 1 Counties in the USA where Persicaria perfoliata was reported during different time intervals

found to be shorter with lower biomass but higher seed height of North American P. perfoliata, and the weevils output than Chinese populations and the specialist introduced into North America originated from adults herbivore Rhinoncomimus latipes Korotyaev (Cole- collected in Hunan Province (Hough-Goldstein et al. optera, Curculionidae) had a greater effect on P. per- 2009; Guo et al. 2011). foliata plants from North America than China (Guo In tests conducted in China and in quarantine in the et al. 2011). U.S., R. latipes showed only minor adult feeding on a few Polygonaceae and did not feed at all on any plant species outside the family (Colpetzer et al. 2004a; Rhinoncomimus latipes, the mile-a-minute weevil Price et al. 2003). There was no egg-laying or larval survival on any host except P. perfoliata. Based on Among the insects found by Ding et al. (2004) feeding these results, a permit for field release in North on P. perfoliata, the only one that has so far passed America was issued by USDA APHIS in July 2004, through the ‘‘filter of safety’’ for potential biological eight years after the start of the program. control agents is R. latipes (Frye et al. 2010). This There are many plant species in the family Polyg- species occurs over a wide geographic range in China onaceae, including the crop species buckwheat (Fag- (Ding et al. 2004). Weevil populations originating in opyrum esculentum Moench) and a few native northeastern (Heilongjiang), central (Hubei), and south- congeners of P. perfoliata, notably P. arifolia (L.) ern (Hunan) provinces were assessed for their impact on Haraldson and P. sagittata (L.) H. Gross, both of P. perfoliata from China and from North America (Guo which co-occur with mile-a-minute weed. However, et al. 2011). Weevils from Hunan Province were found P. perfoliata is morphologically and chemically to be most effective in reducing biomass and plant different from its closest relatives (Park, 1987; Sun 123 J. Hough-Goldstein et al. and Sneden 1999), which increases the likelihood May or June until mid-August, when progressively of finding an insect that feeds on the target but not fewer quadrats had eggs present. By mid-September its native relatives. Nevertheless, of all the insects no eggs were present, although weevils remained collected and tested, R. latipes seems likely to remain active, suggesting that the weevils were entering a the only one that is sufficiently host-specific to pass the reproductive diapause in preparation for overwinter- current stringent requirements for permission to ing. The decline in egg production occurred in near release non-native insects in the U.S. (APHIS 2011; temporal synchrony during each of three years, even Ding, personal communication). though fall temperatures differed among the years. Rhinoncomimus latipes is closely associated with Thus response to photoperiod (or response to plant its host plant at all stages, which probably contributes quality, itself in response to photoperiod) was the most to its extreme host-specificity. Eggs are laid on the likely trigger for diapause induction (Lake et al. 2011). leaves, stems, or buds of the plant and hatch in about 3–5 days, and newly hatched larvae quickly bore into the stem at nodes, feeding internally. Once they are Impacts on P. perfoliata full grown, larvae crawl or drop out of the stem and pupate in the soil under the host plant. Adult weevils The impact of weevils on P. perfoliata was initially emerge from the soil about one week later, crawl up studied using simulated damage based on quarantine nearby stems and mate on the host plant, feed on its observations (Colpetzer et al. 2004b) and subse- leaves, and initiate egg-laying (Colpetzer et al. 2004b; quently in the field with single plants isolated in Hough-Goldstein et al. 2008a; Price et al. 2003). weevil-proof cages. A 2005 pilot study in the absence The complete R. latipes life cycle from egg to adult of weevils found a highly significant difference in both takes about 26 days under laboratory conditions (Price seed production and plant dry weight depending on et al. 2003), and at least 3–4 overlapping generations sun exposure, with plants in full noonday sun produc- occur in the field in southeastern Pennsylvania (Lake ing more than 2,200 seeds, compared with fewer than et al. 2011). In the laboratory, females lay between two 500 per plant for plants in partial sun or full shade and four eggs per day, and continue to oviposit at this (Hough-Goldstein 2008). Subsequent tests were run rate for at least 63 days (Colpetzer et al. 2004b), either in full sun or with treatments blocked by sun leading to potentially massive population growth under exposure. favorable conditions. Adults overwinter in the soil or In initial tests with weevils, single plants isolated in leaf litter. field cages were capable of recovering from high levels Adult weevils are about 2 mm long and are black of damage: 20 weevils per plant completely suppressed when they emerge from the soil, but become coated seed production for about nine weeks following the with an orange-brown substance apparently derived initiation of seed production by control plants (without from plant sap after they have been feeding on weevils), but plants caged with weevils subsequently P. perfoliata for several days. There is some evidence produced large numbers of seeds despite heavy feeding that this substance has a repellant effect on ants (JHG, damage. However, these P. perfoliata plants had all unpublished data), and thus may be important in other plants removed from an area of about 1 m2 avoiding predation. So far there is no evidence for around them, and were much more robust than plants significant predation or parasitism on the weevils in growing naturally nearby, with normal inter- and intra- the introduced range. specific plant competition. The following year the test Weevil behavior in the field was studied at three was repeated but with plants other than mile-a-minute release sites beginning in the spring of 2005 (Lake allowed to grow to a height of about 30 cm in each cage et al. 2011). At each of these sites, 450 weevils were surrounding the focal P. perfoliata plant. Under these released in the center of an array of monitoring somewhat more natural conditions, mortality of P. quadrats arranged in concentric circles out to a perfoliata was over 60% by early August in cages with distance of 25 m from the center. These were sampled 10, 20, or 40 weevils per plant, while fewer than 10% of each week during most of 2005, and every two weeks the control plants died (Hough-Goldstein et al. 2008b). during 2006–2010. Eggs were found in the majority of Seed production in the surviving plants was again quadrats with adult weevils, at every sample date from greatly delayed in the caged plants with weevils. 123 Status of an ongoing biological control program

In addition, there was a clear indication of loss of apical 1200 dominance in the plants with weevils, probably due to dry 1000 the destruction of the terminals by internal larval feeding and adult feeding on capitula (terminal struc- 800 tures associated with flowers or fruits; Colpetzer et al. 600

2004b). Plants with weevils produced many more 400 small side terminals compared with undamaged plants biomass (g) 200 (Hough-Goldstein et al. 2008b). Although this can be an adaptive response by a plant faced with destruction of its perfoliata Persicaria 0 apical terminal, and can even lead to production of more D-Sun D-Shade Sun Shade seeds than undamaged plants (Benner 1988), for a vine Fig. 2 Average dry biomass of Persicaria perfoliata from plots this is generally not a useful response, since it makes the in full sun and under 60% shade cloth, with and without plant less capable of climbing over other plants to reach dinotefuran insecticide treatment (indicated with D; N = 5 plots per treatment; means ± SE). Dinotefuran treatment affected the sunlight (Irwin and Aarssen 1996a, 1996b). In the biomass in sun, not in shade, while shade treatment affected field, heavily damaged individual P. perfoliata can be biomass in the dinotefuran treatment, not in untreated plots quickly overtaken by surrounding plants, leading to (factorial ANOVA, LS Means, P B 0.05; Hough-Goldstein and death of P. perfoliata before seed is produced (personal LaCoss 2011) observation; Hough-Goldstein et al. 2008b). Similarly, in situations where late summer drought occurs, the arrays, moving 15–25 m from the central release point shallow-rooted mile-a-minute plants can be the first to over the course of the season, with an average die, especially where they are stressed by weevil feeding dispersal rate of between 1.5 and 2.9 m per week (Hough-Goldstein et al. 2009). from mid-June through early October (Lake et al. Finally, observations in the field have suggested that 2011). Although weevils are rarely observed flying mile-a-minute weed growing in shaded areas has less in the field, some clearly dispersed through flight, weevil damage than plants growing in full sun, and two because in October of the first year weevils were found experiments were conducted to examine the interactive more than 200 m away from the array, on effects of light environment and herbivory on P. mile-a-minute plants located across a tree line and perfoliata growth (Hough-Goldstein and LaCoss hay fields. By July of the second year weevils were 2011). In 2008, shade cloth that blocked 40% of found 600–700 m from the release site (Lake et al. sunlight was applied to 292 m plots paired with 2011). Spring seedling counts of P. perfoliata gener- unshaded plots in an area with an established weevil ally declined at the three sites from year one to year population. In 2010, the experiment was repeated but three, but in the fourth year there was some increase in as a factorial, in which both sun and shade plots (here mile-a-minute seedling numbers (Fig. 3), probably covered with shade cloth blocking 60% of sunlight) due to a very cold and wet spring in 2009. Mile-a- were included with intact weevil populations and minute seedling counts remained elevated at two of the with weevils eliminated using dinotefuran (SafariÒ), a sites in 2010 (Fig. 3), but by later that season systemic neonicotinoid insecticide. Both years there P. perfoliata cover had declined significantly at all were more weevils and more larval feeding damage in three sites in comparison to 2009 (Lake 2011). the sun than in the shade. In 2010, when mile-a-minute Rhinoncomimus latipes have been reared since weed was harvested from the plots in mid-August, the 2004 at the New Jersey Department of Agriculture plots in the sun where weevils had been eliminated Phillip Alampi Beneficial Insect Rearing Laboratory produced about twice as much biomass as any other (Hough-Goldstein et al. 2008a). Methods have con- treatment (Fig. 2; Hough-Goldstein and LaCoss 2011). tinually improved, with numbers reared for release increasing to more than 76,000 in both 2009 and 2010 (Hough-Goldstein et al. 2008a; J. DeSio, personal Weevil release, dispersal and monitoring communication). Weevils overwintered and estab- lished at 54 of 56 sites (96.4%) where they were During the first year of release in the three monitored released between 2004 and 2007 (Hough-Goldstein arrays, weevils dispersed throughout most of the et al. 2009). In New Jersey, R. latipes has survived at 123 J. Hough-Goldstein et al.

140 a Laurels greatly reduced by a combination of weevil feeding 120 A A and late summer drought (unpublished data, JHG). 100 The average dispersal rate of R. latipes after the first 80 year (based on releases and non-release recoveries in -1 60 New Jersey) was estimated at 4.3 km year (Hough- AB Goldstein et al. 2009). Although this is a respectable 40 BC C 20 dispersal rate for such a small insect, at that rate it would take more than 100 years to reach the current 2 0 edge of the infestation, and therefore additional 25 b BVA CREP releases have been and will continue to be conducted, A 20 primarily using weevils reared at the New Jersey

15 laboratory. Weevils were released in five states

eedlings/ 0.5m AB BC between 2004 and 2008 (Delaware, Maryland, New 10 BC Jersey, Pennsylvania, and West Virginia); in four 5 C additional states for the first time in 2009 (Connect- icut, New York, Rhode Island, and Virginia); in 0 Massachusetts in 2010; and in North Carolina in 2011. 90 Figure 4 shows the location by county of all R. latipes 80 c BVA Wetland A 70 releases (excluding relocations and weevils used in experiments) through 2010. Persicaria perfoliata s perfoliata Persicaria 60 50 AB 40 AB 30 B B Field host range 20 10 0 Wherever weevils are slated for new release, concern 2006 2007 2008 2009 2010 is expressed about whether they might damage non- host plants. In the summer of 2009, an experiment was Fig. 3 Mean (±SE) number of Persicaria perfoliata seedlings counted in May each year at three replicated release sites (one- conducted in which mile-a-minute weed and 11 other way ANOVA by year at each site, Tukey’s test used for mean potential host plant species were transplanted to a separation, P B 0.05; Lake 2011; Lake et al. 2011) replicated array in a farm field, and ten R. latipes were placed at the base of each plant (Frye et al. 2010). Plants included in the study were the most closely sites that were flooded, mowed, and subject to tidal related native species to P. perfoliata, and other plant flooding (Mark Mayer, New Jersey Department of species that the weevil had fed upon as an adult in Agriculture, personal communication). Releases quarantine studies. The study also included a ‘‘plastic conducted between May and October all resulted in plant,’’ with triangular ‘‘leaves,’’ to determine whether successful establishment. Spring seedling counts and weevils would respond to leaf shape and also the percent cover at one of the monitored New Jersey extent to which non-hosts might retain weevils simply sites, where about 7,000 weevils were released in because of their structure rather than their chemical 2005, were dramatically reduced in only a single year. makeup or nutritional value. Weevils placed at the Mile-a-minute seedlings at the associated control site, base of mile-a-minute weed plants were marked with where weevils were not released, remained high for yellow fluorescent dust, while those placed at the base three years, after which the weevils dispersed into this of non-host plants were marked with red fluorescent site and both seedling counts and percent cover of dust, so their movements could be tracked. Weevils mile-a-minute weed declined (Hough-Goldstein et al. from the non-target plants started to leave the array or 2009). Large populations of weevils developed in the move to P. perfoliata within 3 h, and by 44 h the second year following release. Similar results were likelihood of finding a weevil on a non-target plant found on Pea Patch Island, Delaware, USA, where a was 3.5% (Frye et al. 2010). No feeding damage or massive mile-a-minute monoculture was apparently oviposition occurred on the non-hosts. 123 Status of an ongoing biological control program

Fig. 4 Counties in the USA where Rhinoncomimus latipes were released, 2004 through 2010

Plant community response community with a low level of P. perfoliata. At the other two sites, exotic plants such as Japanese stilt While reducing populations of the target weed is a grass (Microstegium vimineum (Trin.) A. Camus) and necessary first step in a successful biological control multiflora rose (Rosa multiflora Thunb.) increased in program, the ultimate aim in a natural area is to abundance as mile-a-minute declined (Lake 2011). At restore a diverse native plant assemblage. Therefore the Pea Patch Island site, Delaware, both native plant analysis of the plant community response should be species such as Allegheny blackberry (Rubus allegh- an integral part of program assessment (Morin et al. eniensis Porter), goldenrod (Solidago spp.) and sensi- 2009; Reid et al. 2009; Thomas and Reid 2007). tive fern (Onoclea sensibilis L.), as well as non-native Until recently, few biological control programs have species such as Japanese stilt grass have increased in conducted such assessments, but where they have, abundance where P. perfoliata populations have results have been mixed (Denslow and D’Antonio declined (unpublished data, JHG). Further research is 2005; Lesica and Hanna 2004; Stephens et al. 2009). needed to characterize sites where suppression of mile- Although the mile-a-minute weed biological control a-minute weed through biological control will lead to a program is too new for full assessment of the plant desired outcome versus sites where additional man- community response to reductions in the target agement techniques will be required (e.g. Lym 2005; weed, indications at present are that there will be Seastedt et al. 2008). For mile-a-minute weed, initial considerable variation in outcomes by site. Of the results suggest that both planting a native seed mix three arrays where weevils were released in 2005, by (Cutting 2011) and planting native perennials in 2010 one consisted of a diverse mostly native plant conjunction with use of a pre-emergent herbicide 123 J. Hough-Goldstein et al.

(Lake 2011) along with the biocontrol weevil, can perfoliatum L. (Polygonales: Polygonaceae). Environ contribute to suppression of P. perfoliata and recovery Entomol 33:990–996 Cutting KJ (2011) An integrated approach to the restoration of of the native plant community. areas invaded by mile-a-minute weed (Persicaria perfoli- ata) using herbaceous native seeding. MS Thesis, University of Delaware, Newark, USA Conclusion and future considerations Denslow J, D’Antonio C (2005) After biocontrol: assessing indirect effects of insect releases. Biol Control 35:307–318 Ding JQ, Fu WD, Reardon R, Wu Y, Zhang GL (2004) The host-specific weevil, R. latipes, establishes and Exploratory survey in China for potential insect biocontrol -1 disperses well, at a rate of more than 4 km year after agents of mile-a-minute weed. Polygonum perfoliatum L., the first year of release. There has been no indication in Eastern USA. Biol Control 30:487–495 of non-target impacts. 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