In: Van Driesche, R., et al., 2002, Biological Control of Invasive Plants in the Eastern United States, USDA Forest Service Publication FHTET-2002-04, 413 p.
Pest Status of Weed
Spotted knapweed, Centaurea maculosa Lamarck, is a purple-flowered, herbaceous, perennial weed, living three to five years on average. It infests semiarid range lands in the western United States and roadsides and fields in the eastern part of the country. Infested areas are dominated by the plant, reducing their grazing value and suppressing native plant communities. The plant, originally from Central Asia, has been in North America for over 120 years.
Nature of Damage
Economic damage. Spotted knapweed is a serious problem on rangeland, especially in the western United States. Bucher (1984) estimated that an 800,000 ha infestation in Montana was causing $4.5 million in annual forage losses, and that invasion of 13.6 million ha of vulnerable rangeland in Montana would cost cattle and sheep ranchers $155.7 million of gross revenue annually. Hirsh and Leitch (1996) reported that an 800,000 ha infestation of spotted knapweed, in combination with two knapweeds of minor importance in Montana (diffuse knapweed, Centaurea diffusa Lamarck, and Russian knapweed, Acroptilon repens [L] de Candolle) was causing $14 million in direct negative impacts and $28 million in indirect effects (i.e., reduced regional economy) to the state of Montana. Harris and Cranston (1979) reported that the 30,000 ha infestation in Canada was reducing forage production more than 88%. In the northeastern and northcentral United States, the plant is primarily a problem of roadsides, fields, and waste areas (Hoebeke, 1993); economic impact of the plant in those regions has not been reported.
Ecological damage. Spotted knapweed reduces livestock and wildlife forage (Thompson, 1996; Watson and Renney, 1974), increases surface water runoff and soil sedimentation (Lacey et al., 1989), and lowers plant diversity (Tyser and Key, 1988). Spotted knapweed produces an allelopathic compound that reduces germination of some grass species (Kelsey and Locken, 1987).
Spotted knapweed is native to Europe and western Asia but has become widespread in parts of the United States and Canada. The plant occurs throughout the United States except for Alaska, Texas, Oklahoma, Mississippi, and Georgia (USDA, NRCS, 2001). The plant is a serious invader of rangeland in the Rocky Mountain region. In Montana alone, the plant infests an estimated 1.9 million ha of rangeland and pasture (Lacey, 1989). In Canada, the plant is abundant in British Columbia, and is common in Ontario, Quebec, and the Maritimes (Watson and Renney, 1974).
Background Information On The Pest Plant
The taxonomy of C. maculosa has been detailed by Dostal (1976) and reviewed by Müller et al. (1988) and Müller (1989). Centaurea maculosa is comprised of several subspecies occurring from western Asia to western Europe. The C. maculosa occurring in North America is a short-lived perennial tetraploid (2n=36) that is considered the same as C. biebersteinii de Candolle subsp. biebersteinii (=C. micranthos Gmelin ex. Hayek), a native of western Asia. However, the most widely distributed C. maculosa in Europe is the biennial diploid (2n=18) C. maculosa spp. rhenana (Boreau) Gugler (Dostal, 1976; Müller et al., 1988; Müller, 1989).
early spring, depending upon moisture availability. Seedlings develop into rosettes; plants that have overwintered as rosettes usually produce floral stems the following summer. Stem elongation occurs in June followed by flowering in July and seed dispersal in August.
Spotted knapweed is adapted to a range of habitats and soil types, but is especially well suited to relatively dry sites (Watson and Renney, 1974). In Europe, the plant is most aggressive in the forest steppe but can form dense stands in more moist areas on well-drained soils including gravel, and in drier sites where summer precipitation is supplemented by runoff (Sheley et al., 1998).
Analysis of Related Native Plants in the Eastern United States
The North American plants most closely related to spotted knapweed include safflower (Carthamus tinctorius L.) and possibly the two “knapweeds,” Centaurea americana and Centaurea rothrockii. Recent evaluations, however, suggest the latter two plants should be treated as Plectocephalus americanus (Nutt.) (Müller-Schärer and Schroeder, 1993). The next closest relatives of spotted knapweed are members of the tribe Cardueae, mainly Carduinae (Cirsium and Cynara [e.g., artichoke]). There are numerous Cirsium species native to North America.
History of Biological Control Efforts in the Eastern United States
Area of Origin of Weed
The native range of the spotted knapweed (tetraploid) occurring in North America is eastern Europe and western Asia (Müller et al., 1989).
Areas Surveyed for Natural Enemies
Surveys were conducted throughout Europe and western Asia for natural enemies.
Natural Enemies Found
Schroeder (1985) listed 38 arthropod species that were known to be associated with spotted knapweed in Eurasia. Of these, 12 species were screened and released in North America against the plant (Table 1).
Host Range Tests and Results
The number of plants included in the test plant list for each of the 12 insect species varied, but averaged around 45 test plant species per insect. Most of the plant species used were from the family Asteraceae, but representative species from one or more other families also were often tested. Particular emphasis was placed on plants in the Asteraceae tribe Cardueae which includes the genus Centaurea. The test plant list for Larinus minutus is presented in Table 2 (Jordan, 1995) because it is fairly representative of the plants tested on all 12 insect species. The only plants of economic importance in North America included in the tests were Carthamus tinctorius L. (safflower), Helianthus annuus L., (common sunflower), and Cynara scolymus L. (globe artichoke). None of the insects oviposited or fed on any of these three plants except for Cyphocleonus achates adults which fed slightly on artichoke. The feeding by C. achates was not of concern, however, because no eggs were laid on the plant. In general, attack by all of the insects was restricted to the genus Centaurea, and usually to the subgenus Acrolophus. There has been no report of attack on non-target species by any of the insects since release, although specific surveys have apparently not been conducted.
Of the 12 biological control agent species released against spotted knapweed in the United States, 10 species have been released against spotted knapweed in the eastern United States and five (Table 1) have become established (Hoebeke, 1993; Wheeler, 1995; Mays and Kok, 1996; Wheeler and Stoops, 1996; Lang et al., 1997; Lang, pers. comm.). The root moth, Pelochrista medullana (Staudinger) (Lepidoptera: Tortricidae) and the root moth, Pterolonche inspersa Staudinger (Lepidoptera: Pterolonchidae) were not released in the eastern United States due to insufficient numbers.
Larval feeding causes the formation of hard, woody galls in the receptacle tissue. The galls divert plant nutrients, resulting in reduced seed production in both attacked and unattacked seed heads on a plant. Urophora affinis is currently reducing seed production of spotted knapweed in the Pacific Northwest close to the threshold needed to achieve economic control (Harris and Shorthouse, 1996).
Fly larvae overwinter within galls (one larva per gall) and pupate in May, followed by adult emergence in late June and July. Urophora affinis is generally univoltine although a small percentage (approximately 7%) emerge in August and complete a second generation (Zwölfer, 1970; Gillespie, 1983; Story et al., 1992).
Urophora quadrifasciata (Meigen) (Diptera: Tephritidae)
Columbia in 1972 (Harris, 1980), but not into the United States. However, by the early 1980s, the fly had dispersed into the Pacific Northwest states. Urophora quadrifasciata is now more widely distributed than U. affinis. Urophora quadrifasciata is common in many areas of the northeast and is very abundant in some areas of upstate New York (Blossey, unpub.data). However, U. quadrifasciata numbers remain low in areas where the two Urophora spp. coexist.
Metzneria paucipunctella Zeller (Lepidoptera: Gelechiidae)
emergence in June and early July. Young larvae feed on developing seeds while older larvae feed on mature seeds and mine the receptacle. Older larvae bind several seeds together with silk webbing, which prevents dispersal of those seeds at maturity. Due to strong intraspecific competition, only one larva survives per seed head (Englert, 1971). Each larva destroys an average of eight seeds per seed head (Story et al., 1991a). Larvae also will attack and destroy other seed head insects, including larvae of the two established seed head flies, Urophora spp. (Story et al., 1991a). Metzneria paucipunctella frequently suffers high overwintering mortality.
begin laying eggs the following evening. Adults live for nine to 11 days and each female lays an average of 75 eggs (up to 290), mostly within a four-day period. Larvae hatch in seven to 10 days and begin mining in the epidermal tissues of the root crown. Older larvae mine in the cortex and endodermis tissues and several larvae may develop in the same root. Agapeta zoegana has one generation per year. Studies in Montana indicate the moth is reducing the biomass of knapweed at some sites (Story et al., 2000). Analyses by Clark et al. (2001a) suggest that probability of A. zoegana establishment at release sites is affected by soil type and the shape (patchy, continuous or linear) of the weed infestation.
Cyphocleonus achates (Fahraeus) (Coleoptera: Curculionidae)
Studies by Clark et al. (2001a) suggest that probability of C. achates establishment at release sites is affected by elevation, the shape (patchy, continuous or linear) of the weed infestation, and the number of years in which releases are made.
Larinus minutus Gyllenhal (Coleoptera: Curculionidae)
into the flower head, where they eat seeds and pappus hairs. Larval development is completed in about 28 days followed by a short pupation period (one to two weeks; Jordan, 1995). Adult L. minutus emerge from the seed head in late September and October and feed on knapweed leaves for a short period before entering the soil to overwinter.
Larinus minutus has developed large populations on diffuse knapweed in Washington, Montana, and Oregon, but population increase on spotted knapweed has been slow.
Larinus obtusus Gyllenhal (Coleoptera: Curculionidae)
Larinus obtusus is a small (5 mm) univoltine weevil that attacks the flower heads of spotted knapweed (Groppe, 1992). The weevil is slightly larger than L. minutus. Collected in Romania and Serbia, L. obtusus was introduced into the United States in Montana in 1992 (Story, unpub. data). The insect is established in moderate numbers in Montana.
Adult weevils become active in May and June and eggs are deposited into freshly opened flower heads in July. Larvae hatch in about four days and immediately feed downward into the flower head, where they eat seeds and pappus hairs. Larval development is completed in about 17 days followed by a nine-day pupation period. Adults of the new generation emerge from the seed head in late summer, approximately 30 days after egg deposition. Adults feed on knapweed leaves for a short period before entering the soil to overwinter.
Bangasternus fausti Reitter (Coleoptera: Curculionidae)
Bangasternus fausti is a small (4.5 mm) univoltine weevil that attacks the flower heads of spotted knapweed (Sobhian et al., 1992). The weevil, collected in Greece, was introduced into the United States in 1990 (Rees et al., 1995).
Adults become active in May and June and eggs are deposited (usually singly) on the stems or bracts of flower heads that are 3.0 to 3.5 mm in diameter. Females cover eggs with a black, hard material. Eggs hatch in eight to 12 days and larvae tunnel through the stem until they enter the flower head. Larvae from eggs laid on the flower head tunnel directly into the flower head. Once in the flower heads, larvae consume florets and ovules. Adults of the new generation emerge from the seed head in late summer and later enter the soil to overwinter. The period from egg to adult is about 32 days.
Chaetorellia acrolophi White and Marquardt (Diptera: Tephritidae)
Pupation occurs in May, followed by adult emergence in June and early July. Eggs are deposited into unopened flower heads from June to July. Larvae hatch in about four days and immediately travel to the center of the flower head, where they burrow into florets. Older fly larvae attack several young seeds, additional florets, and parts of the seed head receptacle. The fly has two generations per year. Larvae and pupae of the first generation of C. acrolophi are white, while second generation larvae and pupae are yellow (Groppe and Marquardt, 1989a).
occurs in May, followed by adult emergence in June and early July. Eggs are deposited into flower heads that are beginning to open. Larvae hatch in about four days and immediately burrow into young seeds (one larva per seed). Older larvae attack several young seeds and occasionally feed on the seed head receptacle. Terellia virens often has two generations, depending upon fall weather (Groppe and Marquardt, 1989b).
Evaluation of Project Outcomes
Establishment and Spread of Agents
Of the natural enemy species released against spotted knapweed in the eastern United States and Canada, the following have been established: Urophora affinis (Virginia, New York, Pennsylvania, Minnesota, Wisconsin, Michigan, Quebec); Urophora quadrifasciata (Connecticut, Indiana, Maryland, Massachusetts, Michigan, Minnesota, New Hampshire, New Jersey, New York, Pennsylvania, Rhode Island, Vermont, West Virginia, Wisconsin, and Quebec); Metzneria paucipunctella (Virginia); Agapeta zoegana (Minnesota); and Larinus minutus (Indiana, Minnesota) (Hoebeke, 1993; Wheeler, 1995; Wheeler and Stoops, 1996; Mays and Kok, 1996; Lang et al., 1997; Lang, pers. comm.) (Table 1). Except for the two Urophora species, particularly U. quadrifasciata, dispersal of the knapweed agents has been modest. An assessment of the Urophora spp. spread was conducted in Montana (Story et al., 1987).
Suppression of Target Weed
Effects of imported natural enemies on spotted knapweed densities in the eastern United States have not been examined. However, impact information has been collected at sites in the western United States. Studies in Montana indicate that the two Urophora spp. are reducing spotted knapweed seed production by a minimum of 40% (Story et al., 1989), seed reduction by the Urophora spp. is further increased when M. paucipunctella is present (Story et al., 1991a), and A. zoegana is significantly reducing the biomass of spotted knapweed at some sites (Story et al., 2000). Spotted knapweed density is significantly reduced at two sites in western Montana where C. achates is well established (Story, unpub. data). Clark et al. (2001b) reported that spotted knapweed stem density, at 13 sites in Montana and adjacent states where U. affinis and one or both root feeding species of natural enemies (A. zoegana, C. achates) were established, declined from about 15 plants per m2 in 1991 to1993 to seven plants in 1997 to 1998.
Effects on Native Plants
Neither the impact of these released agents on native, non-target plants, nor the recovery of native plant communities as weed densities decline have been examined.
The economic benefits of biological control have not been realized yet, even in the west where some agents have been established for more than 15 years. However, given the reductions in knapweed density recently observed at localized infestations in Montana, economic benefits should be measurable in many states in the near future.
Recommendations for Future Work
Because of the large infestations of spotted knapweed in the west and the wide distribution in the north central and eastern United States, extensive redistribution of established biological control agents is required throughout much of the country. For preventative purposes, releases of the agents should be made in all states having only small populations of the weed.
The potential of most of the agents has not yet been realized in the west due to the large size of the infestations and the agents‘ modest rate of population increase. The control agents currently established in the United States are probably capable of reducing spotted knapweed densities in most locations.
There will undoubtedly be locations where the biological control agents are not effective. For example, early observations suggest the current complex of biological control agents in North America may not be effective on knapweed growing at higher elevations (>1,800 m). There are several niches on the plant (e.g., meristem, root collar, stems) that are not being exploited by the current agents in North America. If the need for further agents is deemed necessary, exploration for agents should be concentrated in Asia on tetraploid plants, with some emphasis on those agents attacking the currently unoccupied niches and those occurring at higher elevations.
Evaluation of the agents‘ impact is a priority goal now that some agent populations are reaching high levels at some locations in the west. Evaluation efforts may soon be possible at the smaller infestations in the east, especially in the northcentral states where the root insects, A. zoegana and C. achates, have been introduced.
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