Species pairs for the biological control of weeds: advantageous or unnecessary?

C.A.R. Jackson and J.H. Myers

Summary Two or more species of in the same genera have been introduced in some weed biological control programs, either by accident or on purpose, to increase the climatic range distribution of the agents. If the species are ecological equivalents, the introduction of both species will be unnecessary and may be detrimental if competition reduces their overall impacts. If however the species vary in the type of attack or their distributions, the introduction of congeners can be advantageous. In this paper, we review the following cases of species pair releases in the biological control of weeds in North America: the quadrigemina (Suffrian) and (Forster) for St. Johnswort ( perforatum L.); the gallflies Urophora affinis Frfld. and Urophora quadrifasciata (Meig.) for knapweed (Centaurea) species; the weevils bruchi Hustache and Warner for water hyacinth [ crassipes (Mart.) Solms] and the beetles Galerucella pusilla Duftschmidt and Galerucella calmariensis L. for purple loosestrife (Lythrum salicaria L.). In the cases of Chrysolina and Galerucella, the species pairs appear to be complementary for control of the target weeds, with each species providing good control in slightly different habitats and coexisting at some sites. With the Urophora gallflies, one species is more ef- fective than the other, but overall, reduction is greater when both agents are present in combi- nation (although this seed reduction is insufficient for a reduction of the target weed). In the case of the Neochetina beetles, a difference in the ability of the two species to kill plants was apparent, but whether they differed in habitat preferences was less clear. Given the increasing focus on the possible non-target effects of weed biological control introductions, we recommend that greater care be taken to avoid mixed species introductions and that judicious use be made of controlled field experimenta- tion to determine impacts of the species. Molecular studies of species before introduction could help prevent the accidental introduction of multiple species.

Keywords: congeneric, risk, non-target effects, competition, climate, single agent, multiple agents.

Introduction density are not being achieved by the initially intro- duced agent(s). Where two or more agents are released The issue of single vs multiple agent releases in the simultaneously, they should be released in geographi- biological control of weeds has been a subject of much cally distinct areas where the differential success of the debate. Some have asserted that choosing the most ef- agents can be assessed. fective agents will reduce the potential for undesirable The success of biological control agents in reducing non-target effects (Louda et al., 2003). Denoth et al. target plant density depends on factors such as climate, (2002) reviewed cases of successful biological control target weed phenology, nutrient conditions, dispersal of weeds and found that a majority of successes are at- ability, fecundity, and type and level of damage to key tributed to a single agent. They suggest that additional life stages of the plant. In some cases, two species in agents should be introduced only if reductions in plant the same have been introduced even though they are very similar in their interactions with their host plants. This has sometimes been by accident, such as the case of the two species of Urophora and the mix- University of British Columbia, Department of Zoology, 2360-6270 ture of the two species of Galerucella and sometimes University Boulevard, Vancouver, BC, Canada V6T 1Z4. Corresponding author: C.A.R. Jackson . on purpose from different habitats. When the species © CAB International 2008 are difficult to distinguish morphologically, consider-

561 XII International Symposium on Biological Control of Weeds able confusion can occur over the impacts, distributions failed to establish (Hansen et al., 2004). The five spe- and coexistence of each. This is currently the situation cies were introduced because of differences in habitat with Larinus minutus Gyllenhall. and Larinus obtusus preferences, but control of E. esula in shrubby ripar- Gyllenhall. introduced on knapweeds in North America ian areas remains a challenge (Bourchier et al., 2002). (Harris, 2005). Due to the large number of different species released, The competitive exclusion principle predicts that their recent releases and the lack of comparative data two very similar sympatric species cannot occupy the among all combinations, we did not consider this same niche, and therefore, for coexistence, even very group of congeneric species. We also did not consider similar species must have some differences in niche agents currently under consideration for release. The requirements (Hardin, 1960). It is of interest therefore four species pairs discussed in detail below represent to know if differences between congeneric biological a range of habitat (grassland, riparian and aquatic) and control agents contribute to their successful control of target weed types and have (1) established, (2) reached target weeds. For example, if congeneric species act substantial populations, (3) been studied in their non- in a cooperative and complementary fashion to reduce native range and (4) been compared in the literature. plant densities, their introductions would be warranted. The greatest advantage of congeneric biological con- trol agents occurs if differential climatic tolerances Results result in effective control of the host plant across dif- ferent biomes. St. Johnswort, L.: In this paper, we address two questions in regard Chrysolina hyperici (Forster) and to congeneric releases: (1) Is there evidence that both species are necessary for successful biological control? (Suffrian) (2) Do congeneric species exploit different climatic re- The defoliating beetles, C. hyperici and C. quadri­ gions and thus broaden the geographic effectiveness of gemina, comprise two of the five species of biological biological control? control insects established in North America for con- trol of the rangeland weed St. Johnswort (H. perfora­ Methods and materials tum). These two beetles represent some of the earliest attempts at biological control, having been introduced We restricted our analysis to agents released to control in 1945 and 1946, respectively, in the United States weeds in North America, based on studies reported by (Piper, 2004) and in 1951 in Canada (Harris, 1962). Coombs et al. (2004) and Mason and Huber (2002). Of C. hyperici originates from northern and central the 25 weed control programmes reported in Coombs Europe and western Asia. Eggs are laid in the fall (or et al. (2004), 19 (76%) involved the release of more in the spring in the colder continental interior; Piper, than one species of biological control agent , 2004). Larvae hatch and feed on buds and and 10 (40%) involved the release of congeneric spe- and pupate in the soil. Adults emerge in the spring, cies of agents. feed and then enter the soil for summer diapause before For each case of congeneric biological control agent emerging in the fall to mate and lay eggs. releases, we scoured the literature, searching Web of The native range of C. quadrigemina extends further Science using agent species names as the search terms, south from Denmark to North Africa, and this species paying particular attention to papers where the two spe- prefers warmer, drier areas. Both Chrysolina species cies had been compared. We also searched for papers are univoltine and have similar life cycles but slightly in the literature cited sections of each paper to find ad- different phenologies. ditional information. Field and laboratory studies in New Zealand show We excluded from further analysis species pairs or that, for both Chrysolina species, the termination combinations for which clear differences existed be- of summer diapause is triggered by shortening day tween the species in terms of target weeds. We also length. However, C. quadrigemina terminates sum- excluded species that had not yet been established or mer diapause approximately 3 to 4 weeks earlier, at a for which insufficient post-release information was day length of approximately 13.5 h compared to 12.5 h available for appropriate comparisons. In addition, for C. hyperici. C. quadrigemina females reach sexual we excluded the Aphthona flea species released maturity more quickly and therefore oviposit earlier. In for control of leafy spurge, Euphorbia esula L. Five areas with mild winters C. quadrigemina is considered species, Aphthona czwalinae (Weise), Aphthona la­ to be the superior agent since the larvae feed on plants certosa Rosenhauer, Aphthona cyparissiae (Koch), for a longer time than C. hyperici larvae (Schops et al., Aphthona flava Guillebeau and Aphthona nigriscutis 1996). Foudras, have been released in the United States and Early studies in British Columbia by Harris (1962) Canada, and a sixth species, Aphthona abdominalis suggested that C. hyperici could be the superior agent Duftschmidt, has been released in the United States but in areas with early frosts. Since oviposition occurs on

562 Species pairs for the biological control of weeds: advantageous or unnecessary? average a month later than that of C. quadrigemina, Another gall fly, U. quadrifasciata, was accidentally many of the eggs do not hatch until the following released in 1973. U. quadrifasciata oviposits in slightly spring. Thus, a greater portion of the next generation larger, more mature heads, induces the plant to overwinters in the more resistant egg stage, thus escap- form a thin, papery gall in the ovary and also reduces ing winter larval mortality. seed production (Harris, 1980b). In a subsequent assessment, Harris et al. (1969) U. affinis is primarily univoltine, whereas U. quadri­ found C. quadrigemina to dominate in dry subhumid fasciata is partially bivoltine. In Western Montana, the sites, particularly those with Ponderosa pine (Pinus peaks of first-generation emergence of the two species ponderosa Douglas ex Lawson et. C. Lawson), while occur approximately 1 week apart: 25 June for U. affi­ C. hyperici was most effective in moist subhumid sites nis and 2 July for U. quadrifasciata (Story et al., 1992). where Douglas fir [Pseudotsuga menziesii (Mirbel) At the time of fly emergence, the majority of knap- Franco] was present. Both species of beetle were suc- weed flower heads are at the most suitable stage for U. cessful in reducing H. perforatum populations. affinis. Attack by U. affinis stunts the growth of the re- Peschken (1972) compared C. quadrigemina from maining heads so that many do not reach the size ac- British Columbia (BC) with C. quadrigemina from ceptable to U. quadrifasciata (Berube, 1980), and thus California (the original source of the BC introduc- they must disperse to find sites with capitula suitable tions two decades previously) to determine if post- for oviposition for the second generation (Harris and colonization adaptation had occurred. The BC beetles Myers, 1984; Story et al., 1992; Mays and Kok, 2003). laid a larger number of eggs per female, and this could This could account for the broader distribution of increase the number of beetles surviving the harsher U. quadrifasciata in Canada and the United States (Story winters to the next generation. Furthermore, the BC and Coombs, 2004a,b) despite U. affinis being less beetles demonstrated a greater tendency to seek shelter active fliers (Roitberg, 1988). In a survey in Montana, under cold temperature conditions. Although C. hyper­ U. quadrifasciata occurred at almost all sites examined ici appeared initially to be the more effective agent in as compared to U. affinis that was found at approxi- northern latitudes, its intolerance of dry conditions may mately half of the sites (Story et al., 1987). limit its overall effectiveness. Surveys of original release sites in British Columbia Campbell and McCaffrey (1991) similarly con­ have revealed that U. affinis is most often the domi- cluded that, in Northern Idaho, C. hyperici beetles at­ nant species (Harris, 1980a; Myers unpublished data), tack plants in more mesic forested areas, while C. in agreement with predictions made by Story et al. quadrigemina dominates at grassland sites where the (1992). However, because of geographic and annual target weed H. perforatum most commonly occurs. variation in flower head sizes at emergence times, it Overall, it is clear that, worldwide, C. quadrigemina is unlikely that U. affinis will eventually displace U. is responsible for the majority of the reduction in H. quadrifasciata (Berube, 1980). In addition, the super- perforatum populations; however, in areas with very cooling capacity of U. affinis is superior to that of U. cold winters or more mesic sites at higher elevation, C. quadrifasciata (Story et al., 1993), and Nowierski et al. hyperici offers good complementary control (Schops et (2000) conclude that U. affinis is more tolerant to cold al. 1996; Jensen et al. 2002). winter temperatures. This could also help to explain Such prior knowledge of differences in phenology the predominance of U. affinis, particularly at the more and cold hardiness could inform future agent introduc- northerly release sites. tion and redistribution efforts in other biological con- The exception to U. affinis dominance is in southwest trol programmes. Virginia, where surveys have shown that U. quadrifas­ ciata, which was not introduced but is thought to have dispersed from releases in Maryland, now outnumbers Diffuse knapweed, Centaurea diffusa U. affinis. The longer growing season in this area may Lamark, spotted knapweed, Centaurea favour U. quadrifasciata, although it does not appear to stoebe ssp. micranthos (S.G. Gmelin ex have displaced previously established U. affinis popu- Gugler) Hayek and meadow knapweed, lations (Mays and Kok, 2003). Centaurea pratensis Thuill.: Urophora affinis U. affinis, although smaller than U. quadrifasciata (Roitberg, 1988), reduces seed production by 2.4 / Frfld. andUrophora quadrifasciata (Meig.) head in comparison to 1.9 seeds/head for U. quadri­ The gallfly, U. affinis, was released in Canada in fasciata and thus could be considered to be a more ef- 1970 and in the United States in 1973 for the control of fective agent (Harris, 1980a). Myers and Harris (1980) diffuse and spotted knapweed in the genus Centaurea found that overall seed reduction was slightly greater (Harris, 1980a; Story et al., 1987). U. affinis oviposits when both agents were present in combination. As Cen­ in immature flower heads, inducing the formation of taurea is not seed-limited, however, these gallflies have a woody gall in the receptacle, and reduces knapweed not been successful in reducing overall weed density seed production (Harris, 1980b; Shorthouse, 1989). (Myers and Risley, 2000).

563 XII International Symposium on Biological Control of Weeds

Water hyacinth, males. In a study of the beetles in their native range, (Mart.) Solms: Neochetina eichhorniae Blossey (1995) concluded that these very similar spe- Warner and Hustache cies, which make identical use of their shared food re- source, are able to coexist. He proposed that coexistence The weevil N. eichhorniae was released in the could be due to differences in the competitive abilities southern USA in 1972. The adults and larvae feed on of individuals, as proposed by Begon and Wall (1987): water hyacinth (E. crassipes) leaves, often damaging Individual variation, rather than niche differentiation, meristematic tissues, and leaving distinct scars which promotes the coexistence of competing species. limit plant growth. N. bruchi feeds in a similar manner. In a survey of Central New York completed in 2004, Both species are multivoltine (DeLoach and Cordo, 10 years after the initial introduction of the beetles, 1976; Center, 2004). Grevstad (2006) found that G. pusilla was gener- Both Neochetina species are capable of reversibly ally more abundant than G. calmariensis but that the generating and degenerating flight muscles to corre- abundance of G. calmariensis was increasing. Grevs- spond with dispersal and reproductive phases. N. bruchi tad concluded, however, that the two species did not appears to be more sensitive to plant quality and require occupy identical niches and that coexistence could be high nitrogen content to sustain their high fecundity due to the greater dispersal abilities of G. calmariensis, (Spencer and Ksander, 2004). On stressed plants, Cen- which allows the beetle to coexist with an almost iden- ter and Dray (1992) found more N. bruchi with devel- tical competitor, G. pusilla. oped flight muscles thanN. eichhorniae. Differences in McAvoy and Kok (2004) found that the phenologies preferences for oviposition sites may decrease interspe- of both species are almost identical and are well syn- cific competition and lead to complementary effects, chronized with the host plant. One species completes as N. eichhorniae prefers to oviposit on younger more egg development more slowly, while the other species central leaves, while N. bruchi prefers to oviposit on has faster larval development. In contrast to Neochetina older, more outer leaves (DeLoach and Cordo, 1976). beetles, neither beetle species exploits the lower qual- N. bruchi appears to be the superior agent, mainly ity food source of older leaves. because it has a faster population growth rate, the fe- McAvoy and Kok (2004) concluded that, at higher, males lay more eggs and the larvae develop faster. Thus, colder latitudes in North America, the overall better these beetles can kill plants faster than N. eichhorniae cold tolerance of G. calmariensis makes it a superior (DeLoach et al., 1976). The two species occur together competitor. The situation is complex, however, as throughout their native range, although N. eichhorniae G. calmariensis larvae feed more at lower tempera- predominates at warmer latitudes in northern Argen- tures, but G. pusilla larvae may survive better when tina, Paraguay and Brazil. Also, N. eichhorniae is more food is limiting, as they require less food for develop- tolerant to extremely high temperatures for oviposition, ment (McAvoy and Kok, 2007). adult feeding and adult and egg survival. N. bruchi In western Oregon and Minnesota, G. pusilla is the adults, in contrast, survive better at lower temperatures dominant species (Schooler, 1998; L. Skinner, personal (DeLoach et al., 1976). In Florida, N. eichhorniae is communication), although G. calamariensis is more the more widespread agent (Center et al., 1992; Center common at northern locations in Minnesota (L. Skin- et al., 1999), and it is this agent that is most often cred- ner, personal communication). In Michigan, where ited with the control of Eichhorniae crassipes in North mixtures of the two species were originally introduced, America (Goyer and Stark, 1984; Center and Durden, based on morphological identification, only C. calma­ 1986; Center, 1987). riensis currently occur (Landis et al., 2003; D. Landis, It is possible that N. eichhorniae may be more suit- personal commnunication). In Canada, beetles initially able at warmer latitudes, while N. bruchi may be more came from the mixed species stock in the United States. effective at cooler temperatures and under higher nutri- In 2005, it was found that in, Ontario, G. calmariensis ent levels (Heard and Winterton, 2000). dominated sites of mixed releases that had been made in the mid-1990s (J. Corrigan, personal communica- Purple loosestrife, Lythrum salicaria L.: tion). This is similar to observations in Michigan and Galerucella pusilla Duftschmidt and Minnesota but conflicts with the continued dominance of C. pusilla in New York. In western Canada, species G. calmariensis L. identifications were not confirmed but are thought to The defoliating beetles, G. pusilla and Galerucel­ be G. calmariensis (Lindgren et al., 2002; Denoth and la calmariensis were introduced in North America as Myers, 2005). mixed releases in 1992 (Hight et al., 1995). Adults and The difficulty of distinguishing the two Galeru­ larvae feed on the buds and leaves of purple loosestrife cella species complicates analysis, but G. calmarien­ (L. salicaria) killing plants or reducing their vigour in sis seems to be the superior agent in terms of dispersal subsequent years. The two species of beetles are very and persistence particularly in the North. Successful similar in life history strategies and appearance, and biological control apparently occurs with either species they can only be distinguished by dissection of the alone or together.

564 Species pairs for the biological control of weeds: advantageous or unnecessary?

Discussion References

Biological control is highly context-dependent. Agent Begon, M. and Wall, R. (1987) Individual variation and persistence and plant damage depend on target plant competitor coexistence: a model. Functional Ecology 1, nutritional status and phenology. Furthermore, insect 237–241. agents are highly sensitive to local climatic condi- Berube, D.E. (1980) Interspecific competition between Uro­ tions of temperature, precipitation and humidity. With phora affinis and U. quadrifasciata (Diptera: Tephritidae) increasingly variable trends in climate due to global for ovipositional sites on diffuse knapweed (Centaurea diffusa: Compositae). Zeitschrift für Angewandte Ento­ change, having more than one agent could serve as an mologie 90, 299–306. insurance policy against fluctuations in survival due to Blossey, B. (1995) Coexistence of two leaf-beetles in the environmental conditions. same fundamental niche. Distribution, adult phenology The two Chrysolina beetle species seem to offer and oviposition. Oikos 74, 225–234. complementary control of St. Johnswort on a continent- Bourchier, R., Erb, S., McClay, A.S. and Gassmann, A. wide scale. Overall, C. quadrigemina is probably (2002) Euphorbia esula (L.), leafy spurge, and Euphorbia responsible for most of the control of the weed, with cyparissias (L.), cypress spurge. In: Mason, P.G. and Hu- C. hyperici offering complimentary control in more ber, J.T. (eds) Biological Control Programmes in Canada, mesic, higher elevation and forested sites. This pattern 1981–2000. CABI, Wallingford, UK, pp. 346–358. is similar to the latitudinal gradient in Galerucella spp., Campbell, C.L. and McCaffrey, J.P. (1991) Population trends, with control of purple loosestrife by G. pusilla being seasonal phenology, and impact of Chrysolina quadrige­ mina, C. hyperici (Coleoptera, Chrysomelidae), and Agri­ dominant at more southerly locations, and G. calmar­ lus hyperici (Coleoptera, Buprestidae) associated with iensis dominant at more northerly locations. In the case Hypericum perforatum in Northern Idaho. Environmental of the Urophora gallflies, although U. affinis is supe- Entomology 20, 303–315. rior in terms of seed reduction, overall seed reduction is Center, T.D. (1987) Insects, mites, and plant pathogens as slightly greater with the two species, but the seed reduc- agents of waterhyacinth (Eichhornia crassipes (Mart.) tion is insufficient for successful biological control. Solms) leaf and ramet mortality. Journal of Lake and Res­ Caution, however, is advised. In some cases, com- ervoir Management 3, 285–293. petition from an inferior agent can result in reaching Center, T.D. (2004). Waterhyacinth Eichhornia crassipes. In: suboptimal levels of control (Crowe and Bourchier, Coombs, E. (eds) Biological Control of Invasive Plants in 2006). Furthermore, under certain environmental con- the United States. Oregon State University Press, Corva- ditions, it may be best to introduce only one or other lis, OR, USA, pp. 402–413. Center, T.D. and Durden, W.C. (1986) Variation in water hya- of the agents. For example, under high nutrient condi- cinth/weevil interactions resulting from temporal differ- tions, the release of N. bruchi could result in greater ences in weed control efforts. Journal of Aquatic Plant control than the release of N. bruchi in combination Management 24, 28–38. with N. eichhorniae. Center, T.D. and Dray, F.A. (1992) Associations between wa- Along with the risk of achieving sub-optimal con- ter hyacinth weevils (Neochetina eichhorniae and Neo­ trol due to competition from similar species, with each chetina bruchi) and phenological stages of Eichhornia new species introduction comes the risk of non-target crassipes in Southern Florida. Florida Entomologist 75, effects on ecosystems, a subject which has received 196–211. much attention of late (Cory and Myers, 2000; Strong Center, T.D., Dray, F.A., Jubinsky, G.P. and Grodowitz, M.J. and Pemberton, 2000; Louda et al., 2003). We conclude (1999) Biological control of water hyacinth under con- that the best strategy is careful field and laboratory pre- ditions of maintenance management: can herbicides and insects be integrated? Environmental Management 23, release experimentation in the native habitat, followed 241–256. by the evaluation of replicated releases of individual Coombs, E., Clark, J.K., Piper, G.L. and Cofrancesco, A.F. species into geographically distinct areas. Finally, we (2004) Biological Control of Invasive Plants in the United recommend that, in addition to maintaining voucher States. Oregon State University Press, Corvalis, OR, USA. specimens of insect releases, molecular tools for spe- Cory, J.S. and Myers, J.H. (2000) Direct and indirect eco- cies identification be developed so that mixed stocks of logical effects of biological control. Trends in Ecology & species and strains can be identified. Evolution 15, 137–139. Crowe, M.L. and Bourchier, R.S. (2006) Interspecific interac- tions between the gall-flyUrophora affinisFrfld. (Diptera: Tephritidae) and the weevil Larinus minutus Gyll. (Co- Acknowledgements leoptera: Curculionidae), two biological control agents released against spotted knapweed, Centaurea stobe L. J. Cory, A. Janmaat and M. Tseng provided helpful ssp micranthus. Biocontrol Science & Technology 16, comments on the manuscript. C.A.R. Jackson was 417– 430. funded through a Canada Graduate Scholarship from DeLoach, C.J. and Cordo, H.A. (1976) Life cycle and biology the National Science and Engineering Research Coun- of Neochetina bruchi, a weevil attacking waterhyacinth in cil (NSERC) of Canada. Research was funded by an Argentina, with notes on N. eichhorniae. Annals of the NSERC Discovery grant to J.H. Myers. Entomological Society of America 69, 643–652.

565 XII International Symposium on Biological Control of Weeds

Denoth, M. and Myers, J.H. (2005) Variable success of bio- iensis L. (Coleoptera: Chrysomelidae) on Lythrum sali­ logical control of Lythrum salicaria in British Columbia. caria L. and associated plant communities in Michigan. Biological Control 32, 269–279. Biological Control 28, 78–91. Denoth, M., Frid, L. and Myers, J.H. (2002) Multiple agents Lindgren, C.J., Corrigan, J. and De Clerck-Floate, R.A. in biological control: improving the odds. Biological Con­ (2002) Lythrum salicaria L., purple loosestrife (Lythra- trol 24, 20–30. ceae). In: Mason, P.G. and Huber, J.H. (eds) Biological Goyer, R.A. and Stark, J.D. (1984) The impact of Neochet­ Control Programmes in Canada, 1981–2000. CABI, ina eichhorniae on waterhyacinth in southern Louisiana. Wallingford, Oxon, UK, pp. 383–390. Journal of Aquatic Plant Management 22, 57–61. Louda, S.M., Pemberton, R.W., Johnson, M.T. and Follett, Grevstad, F.S. (2006) Ten-year impacts of the biological con- P.A. (2003) Nontarget effects – the Achilles’ heel of bio- trol agents Galerucella pusilla and G. calmariensis (Co- logical control? Retrospective analyses to reduce risk as- leoptera: Chrysomelidae) on purple loosestrife (Lythrum sociated with biocontrol introductions. Annual Review of salicaria) in Central New York State. Biological Control Entomology 48, 365. 39, 1–8. Mason, P.G. and Huber, J.T. (eds) (2002) Biological Control Hansen, R.W., Spencer, D.E., Fornaseri, L., Quimby, P.C., Programmes in Canada 1981–2000. CABI Publishing, Pemberton, R.W. and Nowierski, R.M. (2004) Leafy Wallingford, Oxon, UK, 583 pp. spurge Euphorbia esula (complex). In: Coombs, E, Clark, Mays, W.T. and Kok, L.T. (2003) Population dynamics and J.K., Piper, G.L. and Cofrancesco, A.F. (eds) Biological dispersal of two exotic biological control agents of spot- Control of Invasive Plants in the United States. Oregon ted knapweed, Urophora affinis and U. quadrifasciata State University, Corvallis, OR, USA, pp. 233–262. (Diptera : Tephritidae), in Southwestern Virginia from Hardin, G. (1960) The competitive exclusion principle. Sci­ 1986 to 2000. Biological Control 27, 43–52. ence 131, 1292–1297. McAvoy, T.J. and Kok, L.T. (2004) Temperature dependent Harris, P. (1962) Effect of temperature on fecundity and sur- development and survival of two sympatric species, Gale­ vival of Chrysolina quadrigemina (Suffr.) and C. hyperici rucella calmariensis and G. pusilla, on purple loosestrife. (Forst.) (Coleoptera: Chrysomelidae). The Canadian En­ BioControl 49, 467–480. tomologist 94, 774–780. McAvoy, T. and Kok, L. (2007) Fecundity and feeding of Ga­ Harris, P. (1980a) Effects of Urophora affinis Frfld and lerucella calamariensis and G. pusilla on Lythrum sali­ Urophora quadrifasciata (Meig) (Diptera, Tephritidae) caria. BioControl 52, 351–363. on Centaurea diffusa Lam and Centaurea maculosa Lam Myers, J.H. and Harris, P. (1980) Distribution of Urophora (Compositae). Journal of Applied Entomology 90, 190–201. galls in flower heads of diffuse and spotted knapweed Harris, P. (1980b) Establishment of Urophora affinis Fr- in British Columbia. Journal of Applied Ecology 17, fld. and U. quadrifasciata (Meig.) (Diptera: Tephriti- 359–367. dae) in Canada for the biological control of diffuse and Myers, J.H. and Risley, C. (2000) Why reduced seed produc- spotted knapweed. Journal of Applied Entomology 89, tion is not necessarily translated into successful biologi- 504–514. cal weed control. In: Spencer, N.R. (ed) Proceedings of Harris, P. (2005) Larinus obtusus (Gyll.) Soft-achene feed- the X International Symposium on Biological Control of ing weevil. In: Harris, P. Classical Biological Control Weeds. Montana State University, Bozeman, MT, USA, of Weeds. Agriculture and Agri-Food Canada. Available pp. 569–581. at: http://res2.agr.ca/lethbridge/weedbio/agents/alarobt_e. Nowierski, R.M., Fitzgerald, B.C., McDermott, G.J. and htm (accessed 2 August, 2007). Story, J.M. (2000) Overwintering mortality of Urophora Harris, P., Peschken, D. and Milroy, J. (1969) The status of affinis and U. quadrifasciata (Diptera: Tephritidae) on biological control of the weed Hypericum perforatum in spotted knapweed: effects of larval competition versus British Columbia. Canadian Entomologist 101, 1–15. exposure to subzero temperatures. Environmental Ento­ Harris, P. and Myers, J.H. (1984). Centaurea diffusa Lam., mology 29, 403–412. and C. maculosa Lam., diffuse and spotted knapweed Peschken, D.P. (1972) Chrysolina quadrigemina (Coleoptera: (Compositae). In: Kelleher, J.S. and Hulme, M.A. (eds) Bio­ Chrysomelidae) introduced from California to British Co- logical Control Programmes Against Insects and Weeds in lumbia against the weed Hypericum perforatum: compar- Canada 1969–1980. CAB, Slough, UK, pp. 127–137. ison of behaviour, physiology and colour in association Heard, T.A. and Winterton, S.L. (2000) Interactions between with post-colonization adaption. Canadian Entomologist nutrient status and weevil herbivory in the biological con- 104, 1689–1698. trol of water hyacinth. Journal of Applied Ecology 37, Piper, G.L. (2004). St. Johnswort Hypericum perforatum. In: 117–127. Coombs, E, Clark, J.K. Piper, G.L. and Cofrancesco, A.F. Hight, S.D., Blossey, B., Laing, J. and Declerck-Floate, R. (eds) Biological Control of Invasive Plants in the United (1995) Establishment of insect biological control agents States. Oregon State University Press, Corvalis, OR, from Europe against Lythrum salicaria in North America. USA, pp. 322–334. Environmental Entomology 24, 967–977. Roitberg, B.D. (1988) Comparative flight dynamics of knap- Jensen, K.I.N, Harris, P. and Sampson, M.G. (2002) Hy­ weed gall flies Urophora quadrifasciata and U. affinis pericum perforatum L., St John’s Wort (Clusiaceae). In: (Diptera: Tephritidae). Journal of the Entomological So­ Mason, P.G. and Huber, J.T. (eds) Biological Control ciety of British Columbia 85, 58–64. Programmes in Canada, 1981–2000. CABI, Wallingford. Schooler, S.S. (1998) Biological control of purple loose- UK, pp. 361–368 strife Lythrum salicaria by two Chrysomelid beetles Landis, D.A., Sebolt, D.C., Haas, M.J. and Klepinger, M. Galerucella pusilla and G. calmariensis. MSc thesis. Or- (2003) Establishment and impact of Galerucella calmar­ egon State University, Corvallis, OR, USA, 128 pp.

566 Species pairs for the biological control of weeds: advantageous or unnecessary?

Schops, K., Syrett, P., and Emberson, R.M. (1996) Summer Story, J.M. and Coombs, E. (2004a). Urophora affinis. In: diapause in Chrysolina hyperici and C. quadrigemina (Co- Coombs, E., Clark, J.K., Piper, G.L. and Cofrancesco, leoptera: Chrysomelidae) in relation to biological control A.F. (eds) Biological Control of Invasive Plants in the of St John’s wort, Hypericum perforatum (Clusiaceae). United States. Oregon State University Press, Corvalis, Bulletin of Entomological Research 86, 591–597. OR, USA, pp. 228–229. Shorthouse, J.D. (1989) Modification of flowerheads of dif- Story, J.M. and Coombs, E. (2004b). Urophora quadrifas­ fuse knapweed by the gall-inducers Urophora affinis ciata. In: Coombs, E., Clark, J.K., Piper, G.L. and Cofran- and Urophora quadrifasciata (Diptera: Tephritidae). In: cesco, A.F. (eds) Biological Control of Invasive Plants in Delfosse, E.S. (ed) Proceedings of the VII International the United States. Oregon State University Press, Corva- Symposium on the Biological Control of Weeds. Istituto lis, OR, USA, pp. 229–230. Sperimentale per la Patologia Vegetale (MAF), Rome, Story, J.M., Nowierski, R.M. and Boggs, K.W. (1987) Dis- Italy, pp. 221–228. tribution of Urophora affinis and U. quadrifasciata, two Spencer, D.E. and Ksander, G.G. (2004) Do tissue carbon and flies introduced for biological control of spotted- knap nitrogen limit population growth of weevils introduced to weed (Centaurea maculosa) in Montana. Weed Science control waterhyacinth at a site in the Sacramento-San Joa- 35, 145–148. quin Delta, California? Journal of Aquatic Plant Manage­ Story, J.M., Good, W.R. and Callan, N.W. (1993) Super- ment 42, 45–48. cooling capacity of Urophora affinis and U. quadrifas­ Story, J.M., Boggs, K.W. and Good, W.R. (1992) Voltinism ciata (Diptera: Tephritidae), two flies released on spotted and phenological synchrony of Urophora affinis and U knapweed in Montana. Environmental Entomology 22, quadrifasciata (Diptera, Tephritidae), two seed head flies 831–836. introduced against spotted knapweed in Montana. Envi­ Strong, D.R. and Pemberton, R.W. (2000) Biological control of ronmental Entomology 21, 1052–1059. invading species – risk and reform. Science 288, 1969–1970.

567