1 Successful biological control of diffuse knapweed, Centaurea diffusa by the weevil 2 Larinus minutus: support for the enemy release and the silver bullet hypotheses 3 4 5 6 7 Judith H. Myers 8 Depts. of Zoology and Agroecology 9 University of British Columbia 10 6270 University Blvd. 11 Vancouver, B.C. 12 V6T 1Z4 13 [email protected] 14 phone: 604 822-3957 FAX 604 822-2416 15 16 17 Pam Krannitz 18 Environment Canada 19 Canadian Wildlife Service 20 5421 Robertson Rd. 21 RR 1Delta, BC 22 V4K 3N2 23 24 1 Abstract. Diffuse knapweed, Centaurea diffusa, is a Eurasian plant that has invaded large 2 areas of grassland in western North America. Starting in 1972, and for the next 20 years, 3 11 species of potential biological control agents were introduced on knapweed. 4 Knapweed persisted at high density however. The 12th biocontrol species, the weevil, 5 Larinus minutus, was first introduced and distributed in British Columbia, Canada 6 beginning in the mid-1990s, and were widely distributed in the late 1990’s. Since 2001, 7 knapweed density has declined in areas with Larinus. From previous work we predicted 8 that biological control would only be successful if an agent killed knapweed plants. 9 Larinus adults feed on bolting plants in the spring and are capable of killing them. The 10 persistence of knapweed at sites lacking Larinus confirms that this species is primarily 11 responsible for successful biological control of diffuse knapweed. This biological control 12 success supports the “enemy release hypothesis” that the vigour and invasiveness of some 13 exotic plants is associated with the lack of particular natural enemies in the exotic habitat. 14 It also supports the “silver bullet hypothesis” that a single agent can successfully control 15 a non-indigenous weed. 16 17 18 19 20 21 22 Keywords: Enemy release hypothesis, silver bullet hypothesis, evolution of increased 23 competitive ability, novel weapons hypothesis, biological control, 2 1 INTRODUCTION 2 Approximately a quarter of the plant species in North America are introduced and 3 many of these cause serious economic and environmental damage (review in Myers and 4 Bazely 2003). Several hypotheses have been put forward to explain the invasiveness of 5 introduced plants. First, the “enemy release hypothesis” suggests that a lack of feeding 6 damage by natural enemies allows some introduced plants to become invasive (reviews in 7 Colautti et al. 2004 and Torchin and Mitchell 2004). This hypothesis is difficult to test 8 because both native and exotic herbivores and diseases vary in their impacts on host 9 plants. Surveys of the occurrence of natural enemies are insufficient for rigorous testing 10 of this hypothesis. Experiments are required. 11 A related hypothesis is that introduced plants with few natural enemies become 12 invasive because they devote fewer resources to defence and more to increased size and 13 fecundity. This is the “evolution of increased competitive ability” hypothesis (Blossey 14 and Nötzold 1995). Evidence for this is contradictory (review in Myers and Bazely 15 2003). A third hypothesis for the dominance of exotic plants is the “novel weapons 16 hypothesis” (Callaway and Ridenour 2004), which proposes that root exudates from the 17 invasive plant species reduce the competitiveness of native species that are not adapted to 18 this new interaction. 19 Finally, some exotic species may be good invaders because they are more 20 efficient at using nutrients or soil moisture than native species. For example, species that 21 are particularly efficient at using phosphorous may be competitively superior in new 22 grassland environments (LeJeune and Seastedt 2001). 3 1 If introduced plants become invasive because they lack natural enemies in the 2 exotic habitat, then the addition of insects or diseases from their native habitat should 3 reduce the density of the host plants. These biological control introductions are tests of 4 the enemy release hypothesis. It is unlikely, however, that all species of natural enemies 5 will have a major impact on host plant density. For example, even when seed predators 6 are numerous, they may have little impact on the density of a plant species that is limited 7 by density-related seedling survival and growth (Myers and Risley 2000, Myers and 8 Bazely 2003). Generalist herbivores may feed on plants but not affect their densities or 9 vigour (Maron and Vilá 2001). 10 Important questions in biological control are how many agents are required for 11 success and what types of agents are most successful (Myers 2001, Myers and Ware, 12 2002)? An assumption of biological weed control has been that success will result from 13 the cumulative impact of a number of agents attacking the target weed (Harris 1981, 14 Myers and Bazely 2003). A review of the biological control literature however, shows 15 that over half of the weed control successes have been attributed to the impact of a single 16 agent, a “silver bullet” (Denoth et al. 2002). If successful agents could be predicted in 17 advance, the number of introductions could be decreased and thus, the risk associated 18 with introducing foreign species to new environments (Louda et al. 1997, 2003). We 19 have predicted that successful agents will be those that kill the host plant at a late life 20 stage (Myers and Risley 2000). We report here evidence gathered from the field over a 21 30-year period to evaluate the agents introduced for the biological control of the 22 rangeland invader, diffuse knapweed, Centaurea diffusa. 4 1 Diffuse knapweed, is a prickly, Eurasian aster that was introduced to North 2 America in the early 1900s, and has since spread to over a million hectares of rangeland 3 in western Canada and the United States (Story et al. 2000, LeJeune and Seastedt 2003). 4 Knapweeds are serious rangeland weeds because they are poor forage for cows and they 5 displace grasses (Harris and Cranston 1979). It has been quite resilient to biological 6 control. Since 1972 twelve species of insects have been introduced for biological control 7 (Bourchier et al. 2002) and 10 have become established. In the early years of the 8 knapweed biological control program considerable effort went into the evaluation of the 9 impacts of biological control species in B.C. (Roze 1981, Morrison 1986 and Powell 10 1988). This biological control program was recently reviewed by Bourchier et al. 11 (2002b) and is described in some detail at the following web site, 12 http://res2.agr.ca/lethbridge/weedbio/plant/bdifknap_over_e.htm. 13 The first biological control agents to be widely established were the gall-forming 14 flies in the family Tephrididae, Urophora affinis and U. quadrifasciata (Harris and Myers 15 1984, Myers 1987), the root-boring beetle, Sphenoptera jugoslavica (Powell 1988, 1990) 16 and the moth Metzneria paucipunctella (Harris and Myers 1980). All of these reduced 17 seed production but they had little impact on knapweed density. Field studies and models 18 showed that even high levels of seed reduction would not reduce knapweed density 19 because lower densities improved the survival of young plants and increased seed 20 production (Powell 1990, Myers and Risley 2000). An agent that killed plants was 21 required (Myers and Risley 2000). 22 Three additional Lepidopteran species that feed on knapweed roots were 23 introduced to British Columbia in the 1980s and 1990s. Agapta zoegana, was introduced 5 1 in 1982, distributed through the 1990s and has become widely established. Pelochrista 2 medullana, was first introduced in 1992 but has not thrived following introduction 3 (Bourchier et al. 2002b). Pterolonche inspersa, apparently became established following 4 its initial introduction in 1986 but it has not been monitored (Harris personal 5 communication). The weevil, Cyphocleonus achates has become widely distributed but 6 still at low densities since the original introduction in 1987 even though adult beetles are 7 not capable of flight. Larvae of this weevil feed on the root core, reduce the growth of 8 flowering plants and can kill rosette plants (Bourchier et al. 2002b, Story 2000). In 9 addition two other species of flies that feed on plant ovaries and achenes of knapweeds 10 were introduced but did not establish, Chaetorellia acrolophi and Terellia virens and 11 another achene feeding weevil Bangasternus fausti was released in the USA but not 12 Canada (Bourchier et al. 2002b). 13 Beginning in 1991, two species of weevil, Larinus minutus and L. obtusus were 14 introduced as biological control agents on diffuse and spotted knapweed respectively 15 (Groppe 1992). Adult L. minutus can kill diffuse knapweed plants by feeding on the 16 epidermis of stems and branches of the bolting plants as well as feeding on buds, thereby 17 causing abortion of the buds. The larvae develop in the seed heads. Between 1996 and 18 1999 L. minutus was introduced to 230 new sites in British Columbia and redistribution 19 continued in 2000 and 2001 (B.C. Ministry of Forests, PENWEED reports). Following 20 the widespread establishment of L. minutus, a striking decline of diffuse knapweed has 21 occurred over a broad geographical range. We document this decline of knapweed in 22 British Columbia and relate the success of this biological control program to hypotheses 6 1 described above in regard to the invasiveness of introduced weeds and to the “silver 2 bullet hypothesis” for successful control by a single species of agent. 3 4 METHODS 5 Field monitoring and Study sites 6 Knapweed density and biological control agents have been monitored at 4 long- 7 term sites in British Columbia since 1976 and at 3 additional sites more recently (Figure 8 1).