Title: Impact of biological control agents on Centaurea diffusa (diffuse knapweed) in central Montana Author




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Smith, L.  2004.  Impact of biological control agents on diffuse knapweed

in central Montana, pp. 589-593.  In:Cullen, J.M., Briese, D.T., Kriticos,

D.J., Lonsdale, W.M., Morin, L. and Scott, J.K. (eds),  Proceedings of the

XI International Symposium on Biological Control of Weeds. CSIRO

Entomology, Canberra, Australia.

Title:

Impact of biological control agents on Centaurea diffusa (diffuse knapweed) in central Montana


Author:

Lincoln Smith, Research Entomologist, USDA-ARS Western Regional Research Center, 800 Buchanan Street, Albany, CA 94710. lsmith@pw.usda.gov
Summary

Centaurea diffusa (diffuse knapweed) is a major weed in semiarid regions in the northwestern United States. Investigations on biological control began in the 1960s and have resulted in the release of 13 species of insect biological control agents (most of which also attack spotted knapweed: C. stoebe subsp. micranthos [often reported as C. maculosa]). In Central Montana, three capitulum-feeding insects (Urophora affinis, U. quadrifasciata and Larinus minutus) and three root-feeding insects (Sphenoptera jugoslavica, Agapeta zoegana and Cyphocleonus achates) have become well established. Populations of diffuse knapweed have rapidly declined at study sites at two locations in the presence of high densities of biological control agents. Larinus minutus and the Urophora species infested up to 62% and 59% of capitula, respectively. Cyphocleonus achates, A. zoegana and S. jugoslavica infested up to 64%, 57% and 31% of roots, respectively. By the summer of 2000, some study sites had no mature plants that could be sampled. Impacts of these insect populations on seed production and plant survivorship are discussed.
Running headline: Control of Centaurea diffusa in Montana

Keywords: biological control, Centaurea diffusa, diffuse knapweed, rangeland, success

Introduction.


Centaurea diffusa Lam. (Asteraceae), diffuse knapweed, is an important invasive weed in semiarid regions of the northwestern continental United States and southwestern Canada (Harris and Cranston 1979; Maddox 1979; Sheley et al. 1998; Roché and Roché 1999). The plant presumably originated from Eurasia, and the first North American specimens were discovered in 1907 in alfalfa fields in Washington State (Howell 1959). Since then, the plant has spread exponentially (Fig. 1), and infested 1.4 million ha by 2000 (Duncan 20001). It is an important weed in the states of Colorado, Idaho, Montana, Oregon, and Washington, and it is designated as noxious in 13 states and four Canadian provinces (Rice 2000).

This plant, and its close relative Centaurea stoebe L. subsp. micranthos (Gugler) Hayek (spotted knapweed; often reported in the literature as C. maculosa Lam. or C. biebersteinii DC. [Ochsmann 2001]) have been the target of biological control for over 40 years (Piper and Rosenthal 1995). Thirteen species of insect biological control agents have been introduced (Table 1; Müller-Schärer and Schroeder 1993, Rees et al. 1996, Story and Piper 2001). These species were multiplied and distributed by USDA-ARS, APHIS and Forest Service; USDI-BLM; and by state departments of agriculture, university personnel, and county agents. All of these species have established to one extent or another, and about half of them have become abundant in at least some regions (Story and Piper 2001, E. M. Coombs personal communication).

Diffuse knapweed populations recently appear to be declining at many sites in Colorado, Montana, Oregon and Washington (Seastedt et al. 2003; personal observation; G. L. Piper, E. M. Coombs and R. F. Lang, personal communication). However, because of limited resources and general emphasis on releasing and distributing agents, rather than on investigation, we lack quantitative documentation of the recent impact of these agents. I happened to arrive in Montana just as the insect populations were beginning to impact C. diffusa populations and here report the partial results of two years observations at two locations that were previously heavily infested by this weed.

Methods


Studies were conducted at two locations in Fergus County, Montana where agents had previously been released. Both are in habitat currently (or historically) dominated by ponderosa pine (Pinus ponderosa P. & C. Lawson) at about 1,000 m elevation with annual precipitation of about 35 cm. The Eickhoff site is a grass meadow used for cattle grazing, but was enclosed by a fence in 1990 to protect it as a biological control release site. The Shannon site was historically excavated for gravel. It is gradually reverting to rangeland and deciduous forest and is grazed by cattle. Releases of Agapeta zoegana, Cyphocleonus achates, Larinus minutus, L. obtusus, Pterolonche inspersa, Sphenoptera jugoslavica, Terellia virens, Urophora affinis, and U. quadrifasciata were made between 1990 and 1997 at the Eickhoff site (see also Table 1). At the Shannon site, the same species were released over the same period, with the addition of Bangasternus fausti, and omission of Urophora spp., L. obtusus, and T. virens. Releases generally comprised 50 to 300 insects except that about 10,000 Urophora spp. were released in 1990. By 1995, seed head weevils, primarily L. minutus, were being collected at the Shannon site for redistribution.

Permanent transects were established at the two locations and permanent positions for Daubenmire frames (20 cm x 50 cm) were marked along the transects at 5 m intervals at Eickhoff and at 1 m intervals at Shannon, where tree clumps interfered with long continuous transects. In the second year (1999), data were collected from additional nearby transects. Number of mature plants, rosettes, and bolts (stems with flowers) were recorded in August 1998 and 1999. To estimate insect attack rates, seed heads were collected in Oct. 1998 and roots in June 1999 from haphazardly chosen plants at uniformly spaced intervals adjacent to the transects. Seed heads were held in a refrigerator and dissected during the winter to determine insect infestation, and roots were dissected immediately in the field. Insect identifications were based on morphology of immature stages except for L. minutus, which was sometimes based on exit hole and characteristic flower head damage.



Results and Discussion


Seed heads were heavily infested at both sites: 99% at Shannon and 59% at Eickhoff (Table 2). The most abundant seed head insects were L. minutus at Shannon and Urophora spp. at Eickhoff (primarily U. affinis, which tends to displace U. quadrifasciata under competition [Berube 1980]). A large proportion of roots were damaged at the two sites: 74% at Shannon and 69% at Eickhoff. Some roots were infested by more than one insect and sometimes by more than one species. Cyphocleonus achates was the most abundant root insect at both sites. This weevil appeared to directly kill some plants at the time they began to bolt because the mature larvae had girdled the vascular tissue from the inside.

The knapweed population drastically decreased during the course of this study (Table 3). At Eickhoff, the knapweed population had already decreased substantially below historical levels, and grasses had become a dominant component of the plant community. Grasses composed a much smaller proportion of the canopy at the Shannon site, which is very gravelly, yet the knapweed population decreased to levels similar to those at Eickhoff. Grass species at both sites included Agropyron smithii (western wheatgrass), A. spicatum (bluebunch wheatgrass), Poa pratensis (Kentucky bluegrass), Stipa comata (needle-and-thread), S. viridula (green needlegrass) (McGregor et al. 1986). The Eickhoff site also had Festuca idahoensis (Idaho fescue), Bouteloua gracilis (blue grama), and Deschampsia cespitosa (tufted hairgrass). There were no nearby sites that were not infested with insects for comparison, so these data do not prove that the insects caused this reduction. However, C. stoebe populations being studied in the same region showed no decline during this period (unpublished data).



Centaurea diffusa populations recently appear to be declining at many sites in Colorado, Montana, Oregon and Washington, where insect biological control agents are abundant (Seastedt et al. 2003; personal observation; G. L. Piper, E. M. Coombs and R. F. Lang, personal communication). This decline has been attributed primarily to the impact caused by high densities of the two Urophora flies, L. minutus and S. jugoslavica. In earlier studies in British Columbia, the Urophora flies greatly reduced seed production, but generally not enough to provide adequate control (Cloutier and Watson 1989; Myers et al. 1989). Although S. jugoslavica is widespread in British Columbia, Oregon and Washington, it appears to be unable to control the weed by itself (Powell and Myers 1988; Powell 1989). The impact of L. minutus adults feeding on rosettes in the spring is suspected to be a deciding factor in the decline of C. diffusa in some areas (G. L. Piper and R. F. Lang, personal communication), although this has not been proven. Seastedt et al. (2003) found that in central Colorado within 4 years of the initial releases C. achates infested about as many C. diffusa plants as S. jugoslavica, despite releasing seven times more of the latter species. Cyphocleonus achates was originally expected to attack primarily C. stoebe (Stinson et al. 1994); however, it is clearly an important agent for C. diffusa, at least in habitats that have a sufficiently warm summer to allow the insect to emerge early enough for it to exploit its long oviposition period. Centaurea diffusa, which is usually a monocarpic biennial, generally has a much smaller root diameter than C. stoebe, which is a perennial (Story et al. 2001), so the weevil is likely to cause much more impact on this plant than on C. stoebe.

Unfortunately, the apparently widespread success of biological control agents to control C. diffusa lacks rigorous documentation of the declines in weed density and hard data showing the direct impact of the agents on the weed population. Further study of these agents would be useful to gain a better understanding of why some became abundant while others did not, and which ones contributed to the decline of the weed population. Many of these agents also attack C. stoebe, although this weed still appears to be uncontrolled in this region.



Acknowledgements


Many thanks to M. Mayer and S. Rosenthal (USDA-ARS), V. Roberts and C. Clark (USDI-BLM), and others who established the release sites and released the agents. Permission to conduct these studies on private land was generously provided by W. Eickhoff and J. Shannon.

References


Berube, D.E. (1980) Interspecific competition between Urophora affinis and U. quadrifasciata (Diptera:Tephritidae) for ovipositional sites on diffuse knapweed (Centaurea diffusa: Compositae). Journal of Applied Entomology, 90, 299-306.

Cloutier, D. & Watson, A.K. (1989) Application of modelling to biological weed control. Proceedings of the VII International Symposium on Biological Control of Weeds (ed E.S. Delfosse), 6-11 March 1988, Rome, Italy, pp. 5-16. Istituto Sperimentale per la Patologia Vegetale, Ministero dell'Agricoltura e delle Foreste, Rome, Italy.

Duncan, C.L. (2001) Knapweed management: Another decade of change. Proceedings of the First International Knapweed Symposium of the Twenty-First Century (ed L. Smith), March 15-16, 2001, Coeur d’Alene, Idaho, pp. 1-7. United States Department of Agriculture, Agricultural Research Service, Albany, California.

Harris, P. & Cranston, R. (1979) An economic evaluation of control methods for diffuse and spotted knapweed in western Canada. Canadian Journal of Plant Science, 59, 375-382.

Howell, J.T. (1959) Distributional data on weedy thistles in western North America. Leaflet of Western Botany, 9,17-29.

Maddox, D.M. (1979) The knapweeds: Their economics and biological control in the western states, U.S.A. Rangelands, 1, 139-143.

McGregor, R.L., Barkley, T.M., Brooks, R.E. & Schofield, E.K. (eds). (1986) Flora of the Great Plains. Great Plains Flora Association. University Press of Kansas, Lawrence, Kansas. 1392 p.

Müller-Schärer, H. & Schroeder, D. (1993) The biological control of Centaurea spp. in North America: Do insects solve the problem? Pesticide Science, 37, 343-353.

Myers, J.H., Risley, C. & Eng, R. (1989) The ability of plants to compensate for insect attack: why biological control of weeds with insects is so difficult. Proceedings of the VII International Symposium on Biological Control of Weeds (ed E.S. Delfosse), 6-11 March 1988, Rome, Italy, pp. 67-73. Istituto Sperimentale per la Patologia Vegetale, Ministero dell'Agricoltura e delle Foreste, Rome, Italy.

Ochsmann, J. (2001) On the taxonomy of spotted knapweed (Centaurea stoebe L.). Proceedings of the First International Knapweed Symposium of the Twenty-First Century (ed L. Smith), 15-16 March, 2001, Coeur d’Alene, Idaho, pp. 33-41. United States Department of Agriculture, Agricultural Research Service, Albany, California.

Piper, G.L. & Rosenthal, S.S. (1995) Diffuse knapweed. Biological Control in the Western United States: Accomplishments and Benefits of Regional Research Project W-84, 1964-1989 (eds J.R. Nechols, L.A. Andres, J.W. Beardsley, R.D. Goeden & C.G. Jackson), pp. 237-241. University of California, Division of Agriculture and Natural Resources, Oakland. Publication 3361.

Powell, R.D. (1989) The functional forms of density-dependent birth and death rates in diffuse knapweed (Centaurea diffusa) explain why it has not been controlled by Urophora affinis, U. quadrifasctata and Sphenoptera jugoslavica. Proceedings of the VII International Symposium on Biological Control of Weeds (ed E.S. Delfosse), 6-11 March 1988, Rome, Italy, pp. 195-202. Istituto Sperimentale per la Patologia Vegetale, Ministero dell'Agricoltura e delle Foreste, Rome, Italy.

Powell, R.D. & Myers J.H. (1988) The effect of Sphenoptera jugoslavica Obenb. (Col., Buprestidae) on its host plant Centaurea diffusa Lam. (Compositae). Journal of Applied Entomology, 106, 25-45.

Rees, N.E., Quimby, P.C., Piper, G.L., Coombs, E.M., Turner, C.E., Spencer, N.R. & Knutson, L.V. (eds). (1996) Biological Control of Weeds in the West. Western Society of Weed Science., USDA-ARS, Montana State University, Bozeman, Montana. World Color Printers, Bozeman, Montana.

Rice, P. (2000) Invaders Database. http://invader.dbs.umt.edu/

Roché, B.F., Jr.& Roché, C.T. (1999) Diffuse knapweed. Biology and Management of Noxious Rangeland Weeds (eds R.L. Sheley & J.K. Petroff), pp. 217-230. Oregon State University Press, Corvallis.

Seastedt, T.R., Gregory, N. & Buckner, D. (2003) Effect of biocontrol insects on diffuse knapweed (Centaurea diffusa) in a Colorado grassland. Weed Science, 51, 237-245.

Sheley, R.L., Jacobs, J.S. & Carpinelli, M.F. (1998) Distribution, biology, and management of diffuse (Centaurea diffusa) and spotted knapweed (Centaurea maculosa). Weed Technology, 12, 353-362.

Stinson, C.S.A., Schroeder, D. & Marquardt, K. (1994) Investigations on Cyphocleonus achates (Fahr.) (Col.: Curculionidae), a potential biological control agent of spotted knapweed (Centaurea maculosa Lam.) and diffuse knapweed (C. diffusa Lam.) (Compositae) in North America. Journal of Applied Entomology, 117, 35-50.

Story, J.M. & Piper, G.L. (2001) Status of biological control efforts against spotted and diffuse knapweed. Proceedings of the First International Knapweed Symposium of the Twenty-First Century (ed L. Smith), March 15-16, 2001, Coeur d’Alene, ID, pp. 11-17. United States Department of Agriculture, Agricultural Research Service, Albany, California.

Story, J.M., Smith, L. & Good, W.R. (2001) Relationship among growth attributes of spotted knapweed (Centaurea maculosa) in western Montana. Weed Technology, 15, 750-761.

F
igure 1. Rate of spread of Centaurea diffusa in the northwestern United States (data from Rice 2000)



Table 1. Biological control agents released in North America to control C. diffusa and C. stoebe







First intro-

Releases at study sitesb

Species

Order: family

ductiona

Shannon

Eickhoff

Seed head insects













Bangasternus fausti

Col.: Curculionidae

1990

91,92,94




Chaetorellia acrolophi

Dip.: Tephritidae

1992







Larinus minutus

Col.: Curculionidae

1991

91,92

96

Larinus obtusus

Col.: Curculionidae

1993




95

Metzneria paucipunctella

Lep.: Gelechiidae

1980







Terellia virens

Dip.: Tephritidae

1992




96

Urophora affinis

Dip.: Tephritidae

1973




90

Urophora quadrifasciata

Dip.: Tephritidae

1981




90

Root-feeding insects













Agapeta zoegana

Lep.: Tortricidae

1984

90,96

96,97

Cyphocleonus achates

Col.: Curculionidae

1988

95,97

96,97

Pelochrista medullana

Lep.: Tortricidae

1984







Pterolonche inspersa

Lep.: Pterolonchidae

1986

90,92,96,97

97

Sphenoptera jugoslavica

Col.: Buprestidae

1980

96,98

90

a First introduction of the species to the United States (Rees et al. 1996).

b Year of release omitting first 2 digits (e.g., 90 = 1990).
Table 2. Proportion of C. diffusa roots and seed heads infested by insects at two sites in Fergus County, Montana




Infestation rate




Shannon

Eickhoff

Roots (June 1999)







Agapeta zoegana

20%

17%

Cyphocleonus achates

52%

29%

Sphenoptera jugoslavica

2%

12%

Root damage

74%

69%

No. plants sampled

86

99










Seed heads (Oct. 1998)







Larinus minutus

62%

10%

Urophora spp.

37%

49%

No. seed heads sampled

145

299

Table 3. Decrease of diffuse knapweed at two locations in Fergus County, Montana






Densitya







1998

1999

Reductionb

Eickhoff location










Bolted plants

8.3 + 3.6

2.3 + 0.8

72% *

Bolts

10.3 + 4.4

2.5 + 1.0

76%

Rosettes

10.7 + 3.4

3.5 + 2.2

67%

No. quadrats

6

10
















Shannon










Bolted plants

24.3 + 3.6

2.4 + 0.8

90% **

Bolts

38.6 + 4.4

3.6 + 1.0

91% **

Rosettes

31.0 + 3.4

0.8 + 2.2

98% **

No. quadrats

12

60




a Mean + SE per Daubenmire frame (0.1 m2) on permanent transects.

b One-way ANOVA test of difference between years, * = P < 0.05, ** = P < 0.001.






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