Impact of biological control agents on Centaurea diffusa (diffuse knapweed) in central Montana
Lincoln Smith1
Summary
Centaurea diffusa (diffuse knapweed) is a major weed in semi-arid regions in the north-western 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 (Sphe- noptera 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 survi- vorship are discussed.
Keywords: biological control, Centaurea diffusa, diffuse knapweed, rangeland, success.
Introduction been targets of biological control for over 40 years (Piper & Rosenthal 1995). Thirteen species of insect Centaurea diffusa Lam. (Asteraceae), diffuse knap- biological control agents have been introduced (Table weed, is an important invasive weed in semi-arid 1; Müller-Schärer & Schroeder 1993, Rees et al. 1996, regions of the north-western continental United States Story & Piper 2001). These species were multiplied and south-western Canada (Harris & Cranston 1979, and distributed by USDA–ARS, APHIS and Forest Maddox 1979, Sheley et al. 1998, Roché & Roché Service; USDI–BLM; and by state departments of 1999). The plant presumably originated in Eurasia, and agriculture, university personnel, and county agents. the first North American specimens were discovered in All of these species have established to some extent, 1907 in alfalfa fields in Washington State (Howell and about half of them have become abundant in at 1959). Since then, the plant has spread exponentially least some regions (Story & Piper 2001; E.M. Coombs, (Fig. 1), and infested 1.4 million ha by 2000 (Duncan pers. comm.). 2001). It is an important weed in the states of Colorado, Diffuse knapweed populations recently appear to be Idaho, Montana, Oregon and Washington, and it is declining at many sites in Colorado, Montana, Oregon designated as noxious in 13 states and four Canadian and Washington (Seastedt et al. 2003, personal obser- provinces (Rice 2000). vation, G.L. Piper, E.M. Coombs and R.F. Lang, This plant, and its close relative Centaurea stoebe personal communication). However, because of limited L. subsp. micranthos (Gugler) Hayek (spotted knap- resources and general emphasis on releasing and weed; often reported in the literature as C. maculosa distributing agents, rather than on investigation, we Lam. or C. biebersteinii DC. [Ochsmann 2001]) have lack quantitative documentation of the recent impact of these agents. I arrived in Montana just as the insect 1 USDA-ARS Western Regional Research Center, 800 Buchanan Street, populations were beginning to impact C. diffusa popu- Albany, CA 94710, USA
589 Proceedings of the XI International Symposium on Biological Control of Weeds observations at two locations that were previously slavica, Terellia virens, Urophora affinis, and U. quad- heavily infested by this weed. rifasciata were made between 1990 and 1997 at the Eickhoff site (see also Table 1). At the Shannon site, the Methods same species were released over the same period, with the addition of Bangasternus fausti, and omission of Studies were conducted at two locations in Fergus Urophora spp., L. obtusus, and T. virens. Releases County, Montana, where agents had previously been generally comprised 50 to 300 insects except that about released. Both are in habitat currently (or historically) 10,000 Urophora spp. were released in 1990. By 1995, dominated by ponderosa pine (Pinus ponderosa P. & C. seed head weevils, primarily L. minutus, were being Lawson) at about 1000 m elevation with annual precip- collected at the Shannon site for redistribution. itation of about 350 mm. The Eickhoff site is a grass Permanent transects were established at the two meadow used for cattle grazing, but was enclosed by a locations and permanent positions for Daubenmire fence in 1990 to protect it as a biological control release frames (20 cm × 50 cm) were marked along the site. The Shannon site was historically excavated for transects at 5 m intervals at Eickhoff and at 1 m inter- gravel. It is gradually reverting to rangeland and decid- vals at Shannon, where tree clumps interfered with long uous forest and is grazed by cattle. Releases of Agapeta continuous transects. In the second year (1999), data zoegana, Cyphocleonus achates, Larinus minutus, L. were collected from additional nearby transects. obtusus, Pterolonche inspersa, Sphenoptera jugo- Numbers of mature plants, rosettes, and bolts (stems
160 140
120 100 80 60
40 20 0 1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 Year
Figure 1. Rate of spread of Centaurea diffusa in the north-western United States (data from Rice 2000).
Table 1. Biological control agents released in North America to control Centaurea diffusa and C. stoebe.
Species Order: family First introductiona Releases at study sitesb 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).
590 Control of Centaurea diffusa in Montana with flowers) were recorded in August 1998 and 1999. The Eickhoff site also had Festuca idahoensis (Idaho To estimate insect attack rates, seed heads were fescue), Bouteloua gracilis (blue grama), and collected in October 1998 and roots in June 1999 from Deschampsia cespitosa (tufted hairgrass). There were haphazardly chosen plants at uniformly spaced inter- no nearby sites that were not infested with insects for vals adjacent to the transects. Seed heads were held in a comparison, so these data do not prove that the insects refrigerator and dissected during the winter to deter- caused this reduction. However, C. stoebe populations mine insect infestation, and roots were dissected imme- being studied in the same region showed no decline diately in the field. Insect identifications were based on during this period (unpublished data). morphology of immature stages except for L. minutus, which was sometimes based on exit hole and character- Table 2. Proportion of Centaurea diffusa roots and seed istic flower-head damage. heads infested by insects at two sites in Fergus County, Montana. Results and discussion Infestation rate Shannon Eickhoff Seed heads were heavily infested at both sites: 99% at Roots (June 1999) Shannon and 59% at Eickhoff (Table 2). The most Agapeta zoegana 20% 17% abundant seed-head insects were L. minutus at Shannon Cyphocleonus achates 52% 29% and Urophora spp. at Eickhoff (primarily U. affinis, Sphenoptera jugoslavica 2% 12% which tends to displace U. quadrifasciata under Root damage 74% 69% competition [Berube 1980]). A large proportion of No. plants sampled 86 99 roots were damaged at the two sites: 74% at Shannon and 69% at Eickhoff. Some roots were infested by more Seed heads (Oct. 1998) than one insect and sometimes by more than one Larinus minutus 62% 10% species. Cyphocleonus achates was the most abundant Urophora spp. 37% 49% root insect at both sites. This weevil appeared to No. seed heads sampled 145 299 directly kill some plants at the time they began to bolt because the mature larvae had girdled the vascular Centaurea diffusa populations recently appear to be tissue from the inside. declining at many sites in Colorado, Montana, Oregon The knapweed population drastically decreased and Washington, where insect biological control agents during the course of this study (Table 3). At Eickhoff, are abundant (Seastedt et al. 2003, personal observa- the knapweed population had already decreased tion, G.L. Piper, E.M. Coombs and R.F. Lang, pers. substantially below historical levels, and grasses had comm.). This decline has been attributed primarily to become a dominant component of the plant community. the impact of high densities of the two Urophora flies, Grasses made up a much smaller proportion of the L. minutus and S. jugoslavica. In earlier studies in canopy at the Shannon site, which is very gravelly, yet British Columbia, the Urophora flies greatly reduced the knapweed population decreased to levels similar to seed production, but generally not enough to provide those at Eickhoff. Grass species at both sites included adequate control (Cloutier & Watson 1989, Myers et al. Agropyron smithii (western wheatgrass), A. spicatum 1989). Although S. jugoslavica is widespread in British (bluebunch wheatgrass), Poa pratensis (Kentucky Columbia, Oregon and Washington, it appears to be bluegrass), Stipa comata (needle-and-thread), and S. unable to control the weed by itself (Powell & Myers viridula (green needlegrass) (McGregor et al. 1986). 1988, Powell 1989). The impact of L. minutus adults
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.
591 Proceedings of the XI International Symposium on Biological Control of Weeds feeding on rosettes in the spring is suspected to be a Howell, J.T. (1959) Distributional data on weedy thistles in deciding factor in the decline of C. diffusa in some areas western North America. Leaflet of Western Botany 9,17–29. (G.L. Piper and R.F. Lang, pers. comm.), although this McGregor, R.L., Barkley, T.M., Brooks, R.E. & Schofield, E.K. has not been proven. Seastedt et al. (2003) found that in (eds) (1986) Flora of the Great Plains. Great Plains Flora central Colorado within 4 years of the initial releases, Association. University Press of Kansas, Lawrence, Kansas. C. achates infested about as many C. diffusa plants as Maddox, D.M. (1979) The knapweeds: their economics and biological control in the western states, U.S.A. Rangelands S. jugoslavica, despite releasing seven times more of 1, 139–143. the latter species. Cyphocleonus achates was originally Müller-Schärer, H. & Schroeder, D. (1993) The biological expected to attack primarily C. stoebe (Stinson et al. control of Centaurea spp. in North America: Do insects 1994), but it is clearly an important agent for C. diffusa, solve the problem? Pesticide Science 37, 343–353. at least in habitats that have a sufficiently warm Myers, J.H., Risley, C. & Eng, R. (1989) The ability of plants to summer to allow the insect to emerge early enough for compensate for insect attack: why biological control of it to exploit its long oviposition period. Centaurea weeds with insects is so difficult. Proceedings of the VII diffusa, which is usually a monocarpic biennial, gener- International Symposium on Biological Control of Weeds, ally has a much smaller root diameter than C. stoebe, (ed E.S. Delfosse), pp. 67–73. Istituto Sperimentale per la which is a perennial (Story et al. 2001), so the weevil is Patologia Vegetale, Ministero dell’Agricoltura e delle Foreste, Rome, Italy. likely to have much more impact on this plant than on Ochsmann, J. (2001) On the taxonomy of spotted knapweed C. stoebe. (Centaurea stoebe L.). Proceedings of the First Interna- Unfortunately, the apparently widespread success of tional Knapweed Symposium of the Twenty-First Century, biological control agents to control C. diffusa lacks (ed L. Smith), pp. 33–41. United States Department of Agri- rigorous documentation of the declines in weed density culture, Agricultural Research Service, Albany, California. and hard data showing the direct impact of the agents Piper, G.L. & Rosenthal, S.S. (1995) Diffuse knapweed. on the weed population. Further study of these agents Biological Control in the Western United States: Accom- would be useful to gain a better understanding of why plishments and Benefits of Regional Research Project W-84, 1964–1989, (eds J.R. Nechols, L.A. Andres, J.W. Beardsley, some became abundant while others did not, and which R.D. Goeden & C.G. Jackson), pp. 237–241. University of ones contributed to the decline of the weed population. California, Division of Agriculture and Natural Resources, Many of these agents also attack C. stoebe, although Oakland. this weed still appears to be uncontrolled in this region. 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 Acknowledgements affinis, U. quadrifasctata and Sphenoptera jugoslavica. Proceedings of the VII International Symposium on Biolog- Many thanks to M. Mayer and S. Rosenthal ical Control of Weeds, (ed E.S. Delfosse), pp. 195–202. Isti- (USDA–ARS), V. Roberts and C. Clark (USDI–BLM), tuto Sperimentale per la Patologia Vegetale, Ministero and others who established the release sites and dell’Agricoltura e delle Foreste, Rome, Italy. released the agents. Permission to conduct these studies Powell, R.D. & Myers J.H. (1988) The effect of Sphenoptera on private land was generously provided by W. Eick- jugoslavica Obenb. (Col., Buprestidae) on its host plant hoff and J. Shannon. Centaurea diffusa Lam. (Compositae). Journal of Applied Entomology 106, 25–45. Rees, N.E., Quimby, P.C., Piper, G.L., Coombs, E.M., Turner, References C.E., Spencer, N.R. & Knutson, L.V. (eds) (1996) Biolog- ical Control of Weeds in the West. Western Society of Weed Berube, D.E. (1980) Interspecific competition between Urophora Science. USDA–ARS, Montana State University, Bozeman, affinis and U. quadrifasciata (Diptera:Tephritidae) for ovipo- Montana. World Color Printers, Bozeman, Montana. sitional sites on diffuse knapweed (Centaurea diffusa: Rice, P. (2000) Invaders Database.
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weed (C. diffusa Lam.) (Compositae) in North America. States Department of Agriculture, Agricultural Research Journal of Applied Entomology 117, 35–50. Service, Albany, California. Story, J.M. & Piper, G.L. (2001) Status of biological control Story, J.M., Smith, L. & Good, W.R. (2001) Relationship efforts against spotted and diffuse knapweed. Proceedings among growth attributes of spotted knapweed (Centaurea of the First International Knapweed Symposium of the maculosa) in western Montana. Weed Technology 15, Twenty-First Century, (ed L. Smith), pp. 11–17. United 750–761.
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