Biotic suppression of invasive weeds in Washington state: a half-century of progress

Gary L. Piper1

Summary

Washington state has long employed natural enemies for the management of invasive aquatic and terrestrial plant species infesting state, federal, tribal, and privately owned water bodies and lands. During the last 55 years, a total of 72 natural enemies have been used for the biological control of 30 nonindigenous weeds. Over 85% of the organisms deployed have been insects, the remaining bioagents consisting of fungi, mites, and nematodes. Of these accidental and intentional introductions, 81% have readily established and yielded various levels of suppression against 27 annual, biennial, and perennial weeds. In recent years, populations of Dalmatian toadflax, Linaria genistifolia ssp. dalmatica, diffuse knapweed, Centaurea diffusa, and other undesired plant species have been reduced by a diverse assem- blage of biotic agents.

Keywords: biological control, failure, history, invasive weeds, success, Washington state.

Introduction Of this land area, approximately 5.1 million ha (29.7%) are publicly owned and 12.1 million ha (70.3%) are Humans have altered the composition of the Earth’s owned by private individuals, corporations, and tribal vegetation for several millenia through their deliberate entities. Rangeland and forestland cover almost 75% of or accidental dispersal of plant species beyond their the state, with rangeland accounting for 2.8 million ha native ranges (Williams 1980, di Castri 1989). Unfortu- and forests occupying 2.2 million ha (WRC/WCC nately, many of these introduced species have become 1986). Agriculture, especially the range-based live- highly invasive or “weedy” in their new ranges and stock industry, and forestry enterprises – production, have caused severe economic, ecological, and human processing, and marketing – is worth $28 billion, or health impacts over a wide range of agricultural and about 12% of Washington’s economy (Hasslen & nonagricultural environments by displacing native McCall 2002). plant species and diminishing biodiversity (Kummerow The suppression of undesirable plant populations 1992). Currently, there are over 2000 invasive weed has long been associated with the protection of the species that have established on private, state, tribal, state’s valued croplands, rangelands, and forests, and is and federal lands in the United States (Anon. 1999). essential if agriculture is to be be sustained into the 21st These unruly weeds represent a major factor in the century and beyond. The majority of Washington’s management of all land and water resources, especially weeds are exotic introductions and, as such, are in the western United States. degrading resource areas they occupy and changing The state of Washington is located in the extreme forever the native character of the state. Cost-effective north-western corner of the continental United States. It management of weeds by eradicating new introductions is bounded by the Canadian province of British and preventing further spread of established species Columbia to the north, the Pacific Ocean to the west, serves to maintain weed-free land for crop production and the states of Oregon and Idaho to the south and east, and preserve the multiple-use potential of grazing respectively. The state is divided into 39 counties which lands. It is important to note too that weeds not only encompass an area of 184,674 sq km or 17.2 million ha. threaten the state’s agricultural base but also its water- ways, recreational lands, property values, public health 1 Department of Entomology, Washington State University, Pullman, WA and safety, and the general ecological health and animal 99164, USA . and plant diversity of its native ecosystems as well.

584 Invasive weeds in Washington state

Washington’s noxious weed law (Chapter 17.10 A, 19 Class B and 6 Class C weeds have been targeted RCW) is one of the most comprehensive and systematic for biological control. Biological control agents have of such laws in the United States. The law recognizes also been introduced against cornflower (Centaurea that weed control is the responsibility of the landowner. cyanus L.), Russian thistle (Salsola kali L.), common To ensure a state-wide effort and compliance at the mullein (Verbascum thapsus L.), and moth mullein (V. local level, the law established a network to share the blattaria L.), species not currently included on the state responsibility for weed suppression activities. The list. Only 21% of the weeds on the state list have had Washington State Noxious Weed Control Board natural enemies introduced against them so many (WSNWCB) and the Washington State Department of species are still opportune targets for biologically based Agriculture (WSDA) work cooperatively with 37 control efforts. county weed control boards, 11 weed districts, and other allied state and federal agencies. The WSNWCB Historical perspectives annually develops and adopts a state noxious weed list. This list categorizes non-native, invasive plant species Anyone involved with biological control of weeds into three major classes: A, B, and C – according to the program activities soon learns that the successful seriousness of the threat they pose to the entire state or control of a target plant is the end result of numerous a region thereof. Class A weeds are species with a very collaborative interactions between individuals at the limited distribution or are unrecorded in Washington local, state, national, and international levels (Goeden and represent a serious threat to the state. Their control 1993). This cooperative undertaking is important or eradication is mandated by law. Class B weeds are of during all phases of a program: project selection, limited distribution or are unrecorded in a region of the natural enemy survey and discovery, biological and state and pose a serious threat to the region. In regions host-range studies, importation, release, and establish- where they are threatening, Class B-designates must be ment, and evaluation. Western North America has been controlled. These species may be too abundant in other a highly active centre of biological control of weeds regions for control to be practical or realistic. Class C research and program implementation for decades weeds are species that are widely established in the (Nowierski 1985). Researchers in California, Idaho, state. County weed control boards and districts may Montana, New Mexico, Oregon, Utah, Washington and seek control of Class C species depending on the local Wyoming, along with those in Canada, have forged a threats they pose and the feasibility of suppression. strong partnership to facilitate the biological suppres- There are presently 30 Class A, 62 Class B, and 30 sion of many weeds of regional importance. Consortia Class C weeds on the state noxious weed list of researchers and other interested parties generate the (WSNWCB 2003). long-term funding that is typically required to ensure Washington state has adopted the integrated weed eventual biological control agent acquisition and management (IWM) approach for dealing with many of delivery against undesirable plant species. its identified problem plants. IWM involves the delib- In the western United States, biological control of erate selection, artful integration, and application of weeds programs are administered differently on a state- cost-effective, environmentally safe, and sociologically by-state basis. In some states, primary responsibility acceptable practices for undesirable plant suppression rests with the state department of agriculture or with (Piper 1992, 2003). The goal of IWM is optimization of university scientists; in other states the responsibility is production/protection of a weed-afflicted ecosystem shared by both entities. United States Department of through the concerted use of scientific knowledge, Agriculture, Animal and Plant Health Inspection preventive tactics, monitoring procedures, and applica- Service, Plant Protection and Quarantine (USDA- tion of diverse control methodologies. Weed suppres- APHIS-PPQ) and/or USDA Agricultural Research sive methods are categorized as being preventive, Service (USDA-ARS) personnel also frequently physical, managerial, chemical, and biological (Ross & collaborate with state or university individuals on bioa- Lembi 1985). Of these, biological control has experi- gent introduction and redistribution efforts. In Wash- enced a high level of acceptance and widespread utili- ington, I serve as the university specialist in biological zation throughout Washington State because of the weed control and am responsible for implementing and alien nature of the invasive weed flora. Biological directing program efforts state-wide, with assistance control involves the intentional deployment of various from USDA–APHIS–PPQ, USDA–ARS, WSDA, naturally occurring organisms such as insects, mites, WSNWCB, and county weed control boards/districts or vertebrate animals, and plant pathogens to destroy or other interested parties. This multiagency coordinated effectively diminish established exotic weed popula- effort ensures that owners/managers of weed-affected tions. Excellent reviews of the procedures followed by lands within Washington will benefit from biological practitioners of biological control are provided by control program activities. However, this type of organ- Wilson (1964), Frick (1974), Andres et al. (1976), ized effort has been in place for only about 25 years. Schroeder (1983), Harley & Forno (1992), McFadyen Before the creation of my university position, biolog- (1998) and Clark et al. (2003). In Washington, 1 Class ical control of weeds activity in the state was unfo-

585 Proceedings of the XI International Symposium on Biological Control of Weeds cused, not vigorously pursued, and consequently its tation efforts were begun against eight additional non- potential as a plant management method was unappre- indigenous plant species at that time (Fig. 1). These ciated by the general public. Insects that had been included leafy spurge (Euphorbia esula L.), black approved as weed control agents in the United States (Centaurea nigra L.), brown (C. jacea L.), diffuse (C. were often made available to university entomologists diffusa Lam.), meadow (C. pratensis Thuill.) and or county agricultural extension agents in Washington spotted knapweed (C. maculosa Lam.), rush skeleton- by University of California (Berkeley) or USDA–ARS weed (Chondrilla juncea L.) and Russian thistle (S. entomologists (Albany, California) and released in a kali). During the following decade, cornflower (C. few localities against various weed species (Johansen cyanus), bull (Cirsium vulgare (Savi) Tenore), musk 1957). Unfortunately, very little time and effort was (Carduus nutans L.) and plumeless thistle (C. acan- subsequently expended on intrastate redistribution and thoides L.), poison hemlock (Conium maculatum L.), impact evaluation activities. and Russian knapweed (Centaurea repens L.) were designated for biological control (Fig. 1). From 1990 to 80 the present, six more weed species have been selected as biocontrol targets. These include field bindweed 70 (Convolvulus arvensis L.), Mediterranean sage (Salvia 60 Total weeds aethiopis L.), purple loosestrife (Lythrum salicaria L.), Total bioagents smooth cordgrass (Spartina alterniflora Loisel.), 50 yellow nutsedge (Cyperus rotundus L.), and yellow 40 starthistle (Centaurea solstitialis L.). During the last

Number three decades, the number of new weeds earmarked for 30 biocontrol within the state increased by 66%. Of this 20 mix of exotic plant targets, there are 17 perennials, 9 biennials, and 4 annuals. Ninety-three percent of these 10 occupy terrestrial habitats, the only semi-aquatic or 0 aquatic species being L. salicaria and S. alterniflora. During the past 55 years, 72 natural enemies have been either accidentally (10 species) or intentionally

1940–1950 1950–1960 1960–1970 1970–1980 1980–1990 1990–2000 (62 species) introduced for the suppression of these weedy plants (Fig. 1). Of these organisms, 63 are Decade insects, 5 are fungi, 3 are mites, and one is a nematode. Figure 1. Cumulative summary by decade of the number Within the class Insecta, 37 or 59% of the bioagents of new weed targets and bioagents released in belong to the order Coleoptera, with the families Curcu- Washington. lionidae and Chrysomelidae being represented by 19 and 11 species, respectively. Of the remaining insect A concerted biological control of weeds program species, 13 (20.5%) belong to the order Diptera, 12 effort was initiated in Washington in 1948 with the (19%) to the order Lepidoptera and one (1.5%) to the purposeful introduction of Chrysolina hyperici order Homoptera. The fungi are all Puccinia spp. (Forster) and C. quadrigemina (Suffrian) (Coleoptera: (Uredinales: Pucciniaceae). Within the order Acari, two Chrysomelidae) for the suppression of the rangeland mites belong to the family Eriophyidae and one to the weed St John’s wort (Hypericum perforatum L.) family Tetranychidae. The nematode used as a bioagent (Johansen 1957, Piper 1985). Other weeds reported to is Subanguina picridis Kirjanova & Ivanova (Nema- be under attack by accidentally introduced natural toda: Tylenchidae). Of this diverse array of organisms, enemy species during the 1940–1950 era included 81% have readily established; the fate of another 13% common and moth mullein (V. thapsus and V. blat- has not yet been fully ascertained. Remarkably, only taria), Dalmatian toadflax (Linaria genistifolia spp. 6% of all introduced agents failed to establish. Lack of dalmatica (L.) Maire and Petitmengin), yellow toadflax establishment has been noted for Aceria malherbae (L. vulgaris Mill.), gorse (Ulex europaeus L.), and Nuzzaci on field bindweed, Altica carduorum Guérin- Scotch broom (Cytisus scoparius (L.) Link (Fig. 1). No Méneville on Canada thistle, Hyles euphorbiae (L.) on new weeds were worked on during the 1950–1960 time leafy spurge, Microlarinus lareynii (DuVal) and M. interval. Between 1960 and 1970, Canada thistle lypriformis (Wollaston) on puncturevine, Pterolonche (Cirsium arvense (L.) Scop.), puncturevine (Tribulus inspersa Staudinger on diffuse and spotted knapweed, terrestris L.), and tansy ragwort (Senecio jacobaea L.) Puccinia canaliculata (Schweinitz) Lagerh. on yellow represented new weeds selected for bioagent releases nutsedge, S. picridis on Russian knapweed, and Zeuxi- (Fig. 1). A notable increase in program activity during diplosis giardi (Kieffer) on St John’s wort. the late 1970s was linked to the establishment of the biological control of weeds specialist position. Impor-

586 Invasive weeds in Washington state

Program successes (Germar), and stem-boring weevil Mecinus janthinus Germar (Coleoptera: Curculionidae). Of these natural Using the terminology of Hoffman (1995), complete enemies, M. janthinus has proven to be the most control success achieved by employing bioagents in damaging thus far. Washington has been achieved against only two weeds, Extensive feeding by M. janthinus adults on succu- L. salicaria and S. jacobaea. Of the remaining 28 target lent foliage and stems of the plant during the spring weeds, substantial success has been recorded against 20 results in the death of stem terminals, thus greatly inhib- of them and negligible success documented against iting potential flower development and seed formation. eight, yielding an overall program success rate of 73%. Numerous eggs are laid in the stems, which the larvae Biological control of weeds program efforts in the state mine within for short distances. Their feeding impairs up until the mid-1980s were previously discussed by plant vigour by reducing carbohydrate supplies, causes Piper (1985). Since then, notable success has been or is premature wilting of stems when xylem vessels are being achieved in the natural enemy-induced suppres- severed, and suppresses flower-bud formation. A 2001 sion of populations of several non-indigenous plant survey (G.L. Piper, unpublished data) of several Wash- species, two of which are profiled herein. ington counties bordering Canada indicated the occur- rence of the insect as a consequence of its immigration Dalmatian toadflax, Linaria genistifolia into the United States from nearby British Columbia spp. dalmatica release sites where it first established during the mid- 1990s (De Clerck-Floate & Harris 2002). Large weevil Dalmatian toadflax, a plant of Eurasian origin, was populations have successfully suppressed Dalmatian intentionally introduced into Canada and the United toadflax stands at some sites both in Canada (De Clerck- States in the mid-1890s for its ornamental and medicinal Floate & Harris 2002) and Washington. Extensive intra- value (Alex 1962). It quickly escaped from its garden state redistribution of this highly effective bioagent into confines and spread to infest North American farmland, other weed-plagued counties commenced in 2002 and pastures, rangeland, and transportation rights-of-way will be continued into the foreseeable future. Additional where it has become a liability. Dense populations of the natural enemy species will be released against the weed short-lived herbaceous perennial weed occur in Wash- as they become available. ington. Vegetative reproduction can give rise to patches of the weed that can persist at a site for many years (Robocker 1974). The plant is also a prolific seed Diffuse knapweed, Centaurea diffusa producer, a several-year-old plant often producing up to Diffuse knapweed, a Eurasian biennial or short-lived a half million seeds, many of which may remain viable perennial accidentally introduced into Washington in the soil for nearly a decade (Robocker 1974). during the early 1900s as an alfalfa seed contaminant, The first biological control program targeting this has since become one of the most serious rangeland and weed was begun in 1960. Field surveys for arthropods forest weeds in the state (Roché & Roché 1988). The associated with the plant were contracted for by the then plant’s seed output is enormous and its infestations are Canada Department of Agriculture (now Agriculture extensive. Efforts to biologically suppress the weed and Agri-Food Canada) and performed by scientists have been underway since 1973 in the United States affiliated with the then Commonwealth Institute of and have culminated in the introduction and release of Biological Control (subsequently the International Insti- 10 seed head- and root-infesting organisms (Story & tute of Biological Control, and now CABI Bioscience) Piper 2001). Of these, the curculionid Larinus minutus (Harris & Carder 1971, Harris 1984). A complex of Gyllenhal is unequivocally the most destructive bioa- insects was discovered, and one of them, the flower and gent established thus far in Washington. foliage-feeding moth, Calophasia lunula (Hufnagel) During the spring and early summer, large popula- (Lepidoptera: Noctuidae), was evaluated and eventually tions of adult weevils feed on the foliage, shoots, and released in Canada and the United States (Harris & immature flower buds of plants. Such feeding may lead Carder 1971, Piper 1985). Although well-established in to outright mortality, especially of seedling and rosette a number of areas of Washington, it has not significantly stage plants, or, if attacked bolted plants survive, diminished weed population abundance. pronounced stunting and flower head deformation typi- Foreign exploration and host-specificity studies on cally result. Plants that escape extensive feeding injury Dalmatian toadflax bioagents were continued during are selected by the females for oviposition. Eggs are the 1980s and 1990s (Rees et al. 1996.). This effort deposited among the pappus hairs and the emergent resulted in the eventual approval for release in North larvae consume developing seeds and receptacle tissue America of the flower-feeding beetle Brachypterolus within the heads. In areas where L. minutus has become pulicarius (L.) (Coleoptera: Nitidulidae), root-boring well-established, the larvae often destroy every seed moths Eteobalea intermediella Riedl and E. serratella head in a stand of diffuse knapweed. It readily survives Treitschke (Lepidoptera: Cosmopterygidae), root- in most sites where it is introduced and attains large galling weevil Gymnetron linariae Panzer, seed- population densities very rapidly, being capable of attacking weevils G. antirrhini (Paykull) and G. netum severely impacting C. diffusa populations within three

587 Proceedings of the XI International Symposium on Biological Control of Weeds to five years after release. The weevil also possesses an BCPC Symposium: Weeds in a Changing World, pp. 77–89. excellent dispersal capability, enabling it to quickly British Crop Protection Council, Farnham, UK. locate and colonize new weed infestations (Whaley Johansen, C.A. (1957) History of biological control of insects in 2002). At numerous sites in Washington, diffuse knap- Washington. Northwest Science 31, 57–79. weed stand densities have been reduced by 95% or Kummerow, M. (1992) Weeds in the wilderness: a threat to biodiversity. Western Wildlands 18, 12–17. more by this bioagent alone. McFadyen, R.E.C. (1998) Biological control of weeds. Annual Review of Entomology 43, 369–393. References Nowierski, R.M. (1985) A new era of biological weed control in the western United States. Proceedings of the VI Interna- Alex, J.F. 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