Weed biological control in California, USA: review of the past and prospects for the future

Michael Pitcairn

doi:10.1007/s10526-018-9884-6

Weed biological control in California, USA: review of the past and prospects for the future

Pitcairn, Michael 2018-05-05 00:00:00 BioControl (2018) 63:349–359 https://doi.org/10.1007/s10526-018-9884-6 Weed biological control in California, USA: review of the past and prospects for the future Michael J. Pitcairn Received: 31 March 2017 / Accepted: 23 April 2018 / Published online: 5 May 2018 The Author(s) 2018 Abstract Weed biological control in California, established, 12 species failed to establish, six species USA began in 1940 with the release of a native scale had their release sites destroyed, and ﬁve species are insect on native Opuntia spp. on Santa Cruz Island, too early to determine. Establishment rate was 82% just offshore from mainland California. Since then, a but the rate differed among taxonomic orders. Indi- total 39 weed species have been targets of biological vidual agents were scored according to level of impact control releases in California. Releases on 11 weed on their host and Coleoptera obtained the highest targets were transfer experiments where agents from average impact score and Diptera the lowest. Mean related weed hosts were released on a new host. Most impact scores over time showed a substantial drop in of the transfer experiment introductions failed but one the 1980s but later increased. Future research efforts weed was successfully controlled. Of the other 28 that emphasize introduction of high impact agents will weeds, release sites for three species were destroyed further support development of this critical weed and for six species releases are too recent to score, but control method for California. for 19 weeds, their level of control was rated as: complete control (three species), substantial control Keywords Weed Biological control California (ﬁve species), and partial (six species), and negligible Establishment rate Success rate control (ﬁve species). Overall, 42% of the projects provide successful control, a result lower than observed in other countries worldwide. Since 1940, 77 species of agents have been released: 54 species Introduction In April 1940, Harry S. Smith, a professor of Handling Editors: Mark Schwarzla¨nder, Cliff Moran and Entomology at the University of California in River- S. Raghu. side, collected crawlers of native Dactylopius tomen- Electronic supplementary material The online version of tosus (Lam.) (Hemiptera: Dactylopiidae) from local this article (https://doi.org/10.1007/s10526-018-9884-6) con- Opuntia spp. near the City of Riverside in southern tains supplementary material, which is available to authorized California, USA carried the live material by boat to users. Santa Cruz Island, located approximately 32 km M. J. Pitcairn (&) offshore from Santa Barbara County, and liberated California Department of Food and Agriculture, them onto two native Opuntia (O. littoralis (Engelm.) Biological Control Program, 3294 Meadowview Road, Cockerell and O. oricola Philbrick (Cactaceae)) Sacramento, CA 95832, USA (Goeden et al. 1967). This action was the ﬁrst use of e-mail: mike.pitcairn@cdfa.ca.gov 123 350 M. J. Pitcairn a live organism to control a weed in North America. Turner (1992), Nechols (1995) and Villegas (1998). Five years later, the leaf beetle, Chrysolina hyperici Details for other projects were obtained in the Annual (Forster) (Coleoptera: Chrysomelidae), was released Reports of the California Department of Food and on Hypericum perforatum L. (Hypericaceae), an Agriculture’s Biological Control Program and in exotic forb that had invaded the pastures and grazing unpublished records at the USDA Agricultural lands in northern California (Holloway 1964). This Research Service’s Quarantine Facility in Albany, second action was the ﬁrst use of an exotic organism to California and the Quarantine Facility at the Univer- control an exotic weed in North America. Since 1940, sity of California, Berkeley. The scientiﬁc names and 77 species of biological control organisms have been taxonomic classiﬁcations of the agents and their weed released on 39 weed species in California. The level of targets were updated and aligned with Winston et al. control that resulted from some of these releases has (2014). The information was entered into two Micro- been spectacular, such as the reduction of H. perfo- soft Excel (version 2013) spreadsheets, one with ratum (Huffaker and Kennett 1959) following the details on the weed targets (Supplementary Table S1) release of the two Chrysolina leaf beetles. Other and one with details on the individual agent species projects have failed to result in any meaningful level (Supplementary Table S2). Summary statistics were of control. generated using the functions of the spreadsheet. In Classical biological control is a weed control generating these two tables, the following deﬁnitions were used. method where host-speciﬁc natural enemies of a weed are introduced from its area of origin to its new area of infestation (Pitcairn 2011). For exotic weeds, this Target weed species involves the introduction of natural enemies of exotic origin. The intention is for the introduced natural For most projects, only one taxonomic entity was enemy to establish, increase in abundance, and, when identiﬁed for each target weed. There are three successful, cause enough feeding damage to substan- exceptions: (1) the three Opuntia taxa, O. littoralis, tially reduce reproduction and recruitment of its host O. oricola, and a hybrid of the two, on Santa Cruz plant. The regional decline of the targeted weed can be Island; (2) Tamarix spp. which, in California, consists dramatic and provides an impressive example of of three species: T. chinensis Lour., T. parviﬂora DC., invertebrate consumers controlling a plant’s abun- and T. ramosissima Ledeb. (Tamaricaceae) as well as dance. This paper describes an attempt to compile a hybrid combinations of all three (Gaskin and Schaal complete list of weed biological control projects in 2003); (3) Centaurea jacea L. (Asteraceae) which California from 1940 through 2015. This review is the consists of three sub-species: C. jacea subsp. jacea, C. ﬁrst comprehensive record of weed biological control jacea subsp. nigra (L.) Bonnier & Layens, and C. research in California and, for some projects, it is the jacea nothosubsp. pratensis (W.D.J. Koch) Celak. For ﬁrst published record. The information obtained on the this analysis, all related taxa within each exception are introduction and establishment of biological control counted as one target weed entity. agents is summarized and an assessment of the success in reducing the abundance of the weed target and the Biological control agent species level of control provided by the established agents is reported. For all agents, only species were counted, different biotypes or other taxonomic entities were not counted separately. For example, two biotypes of Coleophora Materials and methods parthenica Meyrick (Lepidoptera: Coleophoridae) were released against Halogeton glomeratus A list of target weeds and the beneﬁcial organisms (M.Bieb.) C.A. May (Chenopodiaceae): one collected released in California as biological control agents was from Salsola tragus L. (Chenopodiaceae) and another compiled by examining published, peer-reviewed collected from H. glomeratus. For this review, the literature as well as unpublished technical reports release of the two C. parthenica biotypes on H. and quarantine records. Some of the releases associ- glomeratus is counted as one agent-target ated with projects prior to 1990 were summarized in combination. 123 Weed biological control in California, USA: review of the past 351 Number of introductions tragus biotype occurred in 1974 and 1975 (Dunkle 1975) and in 1976, a single release of the H. The number of introductions is the unique combina- glomeratus biotype occurred (Dunkle 1977). The tion of an agent and a target weed. Some agents were focus of the research effort at that time was S. tragus used on more than one weed target and are counted as and the release of the H. glomeratus biotype was a separate introductions. For example, Rhinocyllus one-time event, so, for this analysis, the H. glomeratus conicus (Fro¨lich) (Coleoptera: Curculionidae) was project is considered to be a transfer experiment. introduced on Carduus nutans L. (Asteraceae), Car- duus pycnocephalus L. (Asteraceae), Onopordum Measures of success, weeds acanthium L. (Asteraceae), and Silybum marianum (L.) Gaertn. (Asteraceae). Each of these were counted A common problem in attempting to review the as separate agent-target introductions. success of weed biological control projects worldwide is the lack of quantitative information on the amount Date of introduction of reduction in the target weed (Crawley 1989; Hoffmann 1995; MacFadyen 2000). California has The year of the ﬁrst release of an agent is the year for the same lack of quantitative control information. which a project began. Only a handful of projects, H. perforatum (Huffaker and Kennett 1959), Jacobae vulgaris Gaertn. (Aster- Classical biological control projects and transfer aceae) (Pemberton and Turner 1990), and Chondrilla experiments juncea L. (Asteraceae) (Supkoff et al. 1988) have quantitative before-and-after data on the population A classical biological control project typically consists abundance of the target weed in California. While of ﬁve steps: (1) identiﬁcation of the target weed, (2) these studies are decades old, the lack of resurgence of foreign exploration, (3) host speciﬁcity testing, (4) these weeds does suggest that the results reported may release from quarantine (initial establishment), and (5) still have some relevance. post-release monitoring and redistribution. Ideally, the Hoffmann (1995) proposed three qualitative cate- biological control agent is obtained from the target gories of project success for weed biological control weed in its area of origin and released on the same projects in South Africa: Complete control—when target species in the area of introduction. In some attempts at control are no longer needed in areas where cases, agents from one weed are released on another the agents have established, Substantial control— closely-related weed species to see if the agent where other control efforts are reduced but still provides some beneﬁts. This is particularly true for required to reduce the target weed to acceptable levels agents that have been approved for introduction and over the whole region infested, and Negligible there are other noxious weed species closely related to control—where there has been little or no reduction the target weed in the invaded region. For these in weed abundance or the need to control it. For the projects, the related weed species was not examined in current analysis, a fourth category is added, Partial its area of origin and the released agents were not control—where there is some evidence of decline in obtained from the new target and thereby lack any weed abundance in a limited portion of its infested evolutionary connection and are considered to be range or in some habitats but other control efforts ‘‘transfer experiments.’’ For example, R. conicus was continue with little reduction in use. This last category collected from C. nutans in Italy and released on C. is one level up from Negligible control but below nutans in California where it established. Later, R. Substantial control. It has been included in other conicus weevils were collected from C. nutans in retrospective analyses (Burdon and Marshall 1981; California and released on O. acanthium in California Denoth et al. 2002) and is useful in identifying projects where it failed to establish. The latter introduction is that may have received some beneﬁt from the identiﬁed as a transfer experiment. There is one introduction of biological control agents but the exception: two biotypes of C. parthenica were amount of reduction has not been sufﬁcient to reduce released on H. glomeratus, one reared from S. tragus control efforts by land managers and stakeholders. The and one reared from H. glomeratus. Releases of the S. success ratings are reported as follows: Complete 123 352 M. J. Pitcairn California as an ecoregion control, 3; Substantial control, 2; Partial control, 1; Negligible control, 0. The state of California is one of 48 contiguous states Measures of success, agents that make up the United States of America in the central portion of North American continent. The state The impact of a biological control agent on popula- is located along the western edge of the continent with the Paciﬁc Ocean as its western border. Despite tions of its host plant is dependent on three factors: amount of damage caused by an individual or popu- California being a part of a larger landmass, its unique lation unit of an agent, the local abundance of agents geography (ocean on the west, Sierra Nevada Moun- per individual host plant, and the regional occurrence tains along the eastern border, the Klamath and of the agent over the area infested by the target weed. Cascade Mountains in the north and the Mojave and Sonoran deserts in the southwest) has isolated much of The most successful agents are those that build up large populations on their host plant and inﬂict California from the rest of the continent. For many plant and animal species, these natural geographic sufﬁcient damage to cause a reduction in host abun- dance. Agents that remain scarce in relation to the barriers have limited long-distance colonization and gene ﬂow from close relatives in neighboring areas abundance of their host are unlikely to cause a meaningful reduction in the abundance of their target and this isolation has resulted in a high level of endemism. For example, 57 species of conifers occur weed. Here, an assessment of the level of control (impact) provided by each of the established agents is in California, 27 species are endemic and occur reported. Impact scores for each agent are based on nowhere else in North America or the world (Bakker Klein (2011) and modiﬁed as follows: Trivial: estab- 1971). Overall, it is estimated that 35% of plant lished but remained low in abundance, throughout the species native to California are endemic (Harrison 2013). range of its host, Moderate: obtained a moderate level of abundance in a limited area of its host but was low The climate dominating most of California is Mediterranean, a climate that is rare worldwide and in abundance or absent elsewhere, Considerable: obtained moderate to high levels of abundance in part occurs in only ﬁve other locations: Chile, South Africa, two locations in Australia, and southern or all of the infested range but, alone, was not able to reduce host abundance, Extensive: obtained moderate Europe. Mediterranean climate has cool, wet winters to high levels of abundance that resulted in successful and hot, dry summers. This unusual climate is further control of its host plant, and Unknown: not enough complicated by the extreme length of the summer information is available to make a reasonable decision drought, which lasts longer in California than else- regarding impact or their release occurred too where, and by the unusually high summer tempera- recently. Agent impact is reported as follows: Trivial, tures. During summer, daytime high temperatures commonly exceed 35 C and daytime RH drops below 1; Moderate, 2; Considerable, 3; Extensive, 4; Unknown, U. 10%. Botanists have divided the world landmass into Statistics ﬂoristic regions based on the local level of endemism within the dominant plant communities and the Rates of establishment and impact scores are summa- possibility of shared evolutionary histories of the rized only for those target weeds or agents for which constituent species (Takhtajan 1986). Some regions information is available. For some established agents, are further divided into ﬂoristic provinces and phyto- little or no follow-up has been performed and their geographers have identiﬁed the California ﬂoristic level of control is unknown. In calculating average province as a distinct area separated from other areas rates and scores, information from species with in North America (Takhtajan 1986). As much as 70% of the California Floristic Province is included in the unknown status are not included. political boundary of the state of California (Harrison 2013). It is reasonable, then, to consider California its own ecoregion and that the performance of agents and 123 Weed biological control in California, USA: review of the past 353 Measures of success, weeds the number of successful control projects may not be similar with other areas of North America. Of the 39 weed targets on which biological control agents were intentionally released, 11 were identiﬁed as transfer experiments where agents were obtained Results from closely-related exotic weeds (Supplementary Table S1). Most of the transfer experiment introduc- From 1940 through 2015, 77 species of biological control agents were released on 39 weed targets in tions failed (establishment rate = 32%, 7/(24-2 California (Supplementary Tables S1 and S2). Some unknowns)). However, the releases on C. virgata agents were released on more than one target weed subsp. squarrosa were very successful, where ﬁve of (e.g., R. conicus was released on four target weeds) so, seven agents established and two agents, Larinus minutus Gyllenhal (Coleoptera: Curculionidae) and in total, 101 unique target-agent introductions occurred during this time period. The weed targets Bangasternus fausti (Reitter) (Coleoptera: Curculion- idae), built up high numbers and resulted in a 99% include taxa from 18 families and 12 orders. The family Asteraceae was the most represented with 16 reduction in seed production effectively stopping all plant recruitment (Woods and Villegas 2006). In the species, followed by Euphorbiaceae (three species), Chenopodiaceae (two species), Fabaceae (two spe- years following, adult plants have slowly died from other causes and now C. virgata subsp. squarrosa is cies) and Hypericaceae (two species). The other 13 families (Amaranthaceae, Araceae, Brassicaceae, greatly reduced in abundance and no longer consid- Cactaceae, Hydrocharitaceae, Lamiaceae, Lythraceae, ered an economic weed (Woods and Villegas 2006). In Plantaginaceae, Poaceae, Pontederiaceae, Salvini- evaluating the success of the classical weed biocontrol aceae, Tamaricaceae, Zygophyllaceae) were repre- projects, the 11 weed targets involved in the transfer experiments were removed from consideration. sented with one species each. All plant life histories are represented with perennial species the most In total, 28 weeds have been classical weed biological control targets (Table 1). For nine of these abundant (22 species), followed by biennial (ten species) and annual (seven species). The most com- targets, success was not evaluated. Three projects, Alternanthera philoxeriodes (Mart.) Griseb. (Amaran- mon plant growth form was herbaceous forbs (33 species), followed by shrubs (three species), one grass thaceae), Hydrilla verticillata (L. f.) Royle (Hy- (Arundo donax L. (Poaceae)), one tree (Tamarix spp. drocharitaceae), and Pistia stratoites L. (Araceae) complex) and one target of succulents (Opuntia spp. had each of their study locations destroyed shortly on Santa Cruz Island). The targeted weed species after release of their agents. There are six projects for occurred in a variety of habitats, with rangelands (30 which releases occurred within the last ten years and species) and natural areas (24 species) the most not enough time has elapsed to allow evaluation. A total of 19 weeds are considered further and the level common, followed by aquatic habitats (includes riparian species and free-ﬂoating aquatic macro- of control achieved for each project shows the following results (Table 1): ﬁve weeds showed neg- phytes) (eight species) and managed pastures and cultivated lands (eight species) (the total exceeds 39 ligible control, six weeds are rated as partial control, ﬁve weeds are under substantial control, and three species because some weeds occur in multiple habi- tats). The number of agents released on an individual weeds are under complete control (H. perforatum, the Opuntia spp. on Santa Cruz Island, and J. vulgaris). targeted weed species ranged from one to seven agents, with the Opuntia spp. on Santa Cruz Island, The ﬁve weeds under substantial control (Tribulus Centaurea solstitialis L. (Asteraceae), and Centaurea terrestris L. (Zygophyllaceae), C. nutans, C. juncea, virgata Lam. subsp. squarrosa (Boiss.) Gugler (Aster- Lythrum salicaria L. (Lythraceae), and Salvinia aceae), each receiving the highest number of agents. molesta D.S. Mitch. (Salviniaceae)) are under com- plete control in some areas of their range, but much The rate of agent establishment by weed target ranged from 0 to 100%. However the majority of targets less or little control occurs in other areas of their infestation. For example, L. salicaria is under com- showed intermediate rates of establishment. plete control in area of Big Lake and along the Fall River in eastern Shasta County, an area at 41 latitude 123 354 M. J. Pitcairn Table 1 List classical weed biological control targets in California from 1940 to 2015 Scientiﬁc name Common name Year of 1st Level of Number of Agents introduction control RE C2 C3 Ulex europaeus L. Gorse 1953 0 2 2 1 0 Cytisus scoparius (L.) Link Scotch Broom 1960 0 2 2 1 0 Silybum marianum (L.) Gaertn. Milk Thistle 1969 0 1 1 1 0 Salsola tragus L. Russian Thistle 1973 0 2 2 0 0 Eichhornia crassipes (Mart.) Solms Water Hyacinth 1982 0 4 3 1 0 Centaurea solstitialis L. Yellow Starthistle 1969 1 7 6 1 0 Carduus pycnocephalus L. Italian Thistle 1973 1 1 1 1 0 Centaurea diffusa Lam. Diffuse Knapweed 1976 1 4 4 3 0 ? 2U Salvia aethiopis L. Mediterranean Sage 1976 1 1 1 1 0 ? 1U Centaurea stoebe L. Spotted Knapweed 1993 1 5 5 1 ? 1U 0 Cirsium vulgare (Savi.) Ten. Bull Thistle 1993 1 1 1 1 0 Tribulus terrestris L. Puncturevine 1961 2 2 2 2 2 Carduus nutans L. Musk Thistle 1974 2 1 1 1 1 Chondrilla juncea L. Skeletonweed 1975 2 4 3 ? 1U 2 1 Lythrum salicaria L. Purple Loosestrife 1996 2 4 4 1 ? 3U 1 Salvinia molesta D.S. Mitch. Giant Salvinia 2002 2 1 1 1 1 Opuntia spp. Prickly Pear Cactus 1940 3 7 3 2 1 Hypericum perforatum L. Klamath Weed 1945 3 6 5 2 2 Jacobaea vulgaris Gaertn. Tansy Ragwort 1959 3 3 2 2 2 Cirsium arvense (L.) Scop. Canada Thistle 1966 TE 3 2 0 0 Euphorbia esula L. Leafy Spurge 2001 TE 3 2 0 ? 1U 0 Tamarix spp. Saltcedar 2001 TE 2 1 ? 1U 1 0 ? 1U Linaria dalmatica ssp. dalmatica (L.) Mill. Dalmatian Toadﬂax 2008 TE 1 1 1 0 ? 1U Arundo donax L. Giant Reed 2010 TE 2 1 ? 1U 0 ? 1U 0 Rhaponticum repens (L.) Hidalgo Russian Knapweed 2011 TE 2 0 ? 1U 0 0 Alternanthera philoxeroides (Mart.) Griseb. Alligatorweed 1964 NA 3 Ex – – Hydrilla verticillata (L. f.) Royle Hydrilla 1991 NA 2 Ex – – Pistia stratiotes L. Waterlettuce 2013 NA 1 Ex – – Totals 77 56 ? 4U 27 ? 6U 11 ? 5U For each weed target, the current level of control and the number of agents released, established, and the level of agent impact are reported. Target weeds are listed by order of level of control and year of introduction of ﬁrst agent Opuntia littoralis (Engelm.) Cockerell, O. oricola Philbrick, and hybrids between these two species Tamarix chinensis Lour., T. parviﬂora DC., T. ramosissima Ledeb., and hybrids among these species Level of control of the target weed: 0 = negligible control; 1 = partial control; 2 = substantial control; 3 = complete control; TE = too early to rate; NA = no information available R number of agents released, E number of agents established; C 2 number of established agents with impact scores 2 and higher (from Supplementary Table S2), C 3 number of established agents with impact scores 3 and higher (from Supplementary Table S2), U status unknown, Ex agents extirpated in northern California. However, L. salicaria occurs in photoperiod limitations (unpublished data). The several locations further south in California, including beetles did establish in Butte County, a low elevation tributaries of the Feather River in Butte County, the (35 m) location approximately 80 km south of Big Kings River in Fresno County, and the Kern River in Lake, but the growing season begins before and Kern County. The two Galerucella beetles did not extends after the active period of the beetles, so the establish in areas of California south of 39 latitude plants are able to outgrow the damage (unpublished (e.g., Fresno and Kern counties) because of data). 123 Weed biological control in California, USA: review of the past 355 18 100 Combining the number of weed targets under substantial and complete control, the success rate is 42% (8/19 weed targets). Out of the 58 unique target- agent introductions associated with the 19 classical 60 biological control target weeds (Table 1), 86% of these introductions resulted in establishment of the agent (49/(58-1 unknown)). Each of the 19 target 4 weeds had at least one agent established. When weed 10 0 0 targets are sorted by life history, annual weeds have a lower rate of success (20% of targets under complete or substantial control) compared to the biennial (60%) and perennial (44%) weed targets, a result similar to Number Released % Establishment that reported by Chaboudez and Sheppard (1995) and Fig. 1 Numbers of weed biological control agents released and Straw and Sheppard (1995). rates of establishment in California by decade Measures of success, agents For those agents for which information is available, an assessment of their impact on their host was A total of 77 species have been released as weed recorded (Supplementary Table S2). Two associations biological control agents from 1940 through 2015 are of interest. First, the average impact score by order (Supplementary Table S2). Most species were insects shows the Coleoptera to have the highest average (n = 72) but two mite and three fungal species were score and the Diptera to have the lowest average score also released. Species of Coleoptera were the most (Fig. 2a). Second, the average impact score of agents represented (n = 37), followed by Diptera (n = 13) released varied by decade (Fig. 2b). Interestingly, the and Lepidoptera (n = 12). By family, Curculionidae average impact score showed a substantial drop in the and Chrysomelidae were the most used (n = 17 and 1970s and 1980s, suggesting that, for the agents 12, respectively), followed by Tephritidae (n = 8). All released during this time period, little beneﬁt appears other taxonomic families had four or less species to have come from their presence. introduced. Overall, the establishment rate for agents The combined impact of the complex of agents that on at least one target weed was 82% (54/(77-11(5 established on each weed target was examined by unknowns and 6 extirpated))) but rate of establishment tallying the number of agents that resulted in impact differed among orders and families with the Acari scores of two or higher and the number of agents (two species), Hymenoptera (one species), and fungi having impact scores three or higher (Table 1). The (two species) having the highest rate of establishment results show that for the 28 classical biological control (100%), followed by Coleoptera (83%), Diptera targets 54% (27/(56-6 unknowns)) of established (69%), Hemiptera (67%), and Lepidoptera (55%). agents provided a moderate or higher level of impact The release rate averaged 9.7 species per decade with a on their hosts. Eleven agents are rated with impact lower release rate initially and a notable drop in the scores of three or higher, indicating that 24% (11/(56- 1980s (Fig. 1). However, the rate of establishment 11 unknowns)) of the agents that established are across decades showed an increasing trend with the considered effective agents and contributed to suc- highest establishment rate (88%) obtained in the two cessful control of their hosts. In a review of interna- most recent full decades (1990–2009). Among the tional weed biological control projects, Crawley insect and mite biological control agents, 58% were (1989) reported an average of 25% of established concealed feeders/borers (including seed-feeding agents to be effective, suggesting that the results in insects), 20% were chewers, 14% were sap feeders, California are similar. and 8% were gallers. All plant parts were targeted by the agents with 37% being leaf-feeders, 26% seed/ ﬂower feeders, 22% feeding on roots and lower stems, and 15% feeding on the main/upper part of stems. Number of Agents Released % Establishment 356 M. J. Pitcairn 3.50 that the successful control of Klamath weed in California resulted in a cumulative savings of $14 3.00 million dollars during 1953 through 1959. In Oregon where J. vulgaris is also considered to be under 2.50 complete control, it was estimated that the project 2.00 resulted in an annual savings of more than ﬁve million dollars due to reduced losses to livestock, increased 1.50 productivity of pastures, and reduced herbicide use (Coombs et al. 1996). It is likely that California has 1.00 reaped similar amounts of economic and environmen- tal beneﬁts from each of these classical weed biolog- ical control programs. Despite these successes, there is much more to accomplish. A total of six weeds are considered under partial control and a further ﬁve weeds show little or 3.50 no control (Table 1). In comparison with weed 3.00 biological control programs in other countries, the rate of success for California programs (42%) is low 2.50 (Table 2). Classical weed biological control programs in Australia, New Zealand, and South Africa have 2.00 each achieved rates of success (substantial and com- 1.50 plete control combined) of over 80%. Interestingly, the rate of establishment of introduced agents and the 1.00 proportion of agents that are effective in California are 1940s 1950s 1960s 1970s 1980s 1990s 2000s (n=4) (n=5) (n=6) (n=7) (n=6) (n=9) (n=3) similar to that reported for Australia, New Zealand, and South Africa so the reason for the low success rate Fig. 2 a Average impact value (? SE) of weed biological in California may be due to other factors. Three control agents established in California by taxonomic order. possible explanations are considered. Sample size (number of species) is identiﬁed in the parentheses. Orders with only one species are not displayed. b Average The ﬁrst explanation is that, for many agents, there impact value (? SE) of weed biological control agents released is a mis-match with climate. The Mediterranean in California by decade. Sample size (number of species) is climate which dominates California is unusual world- identiﬁed in the parentheses. Values are calculated from wide and the lack of agents sourced from a Mediter- individual agent data in Supplementary Table S2 ranean region may contribute to the low success rate and the low impact scores for agents that establish. Discussion While many of the weeds targeted for control in California are of European origin, not all weeds occur In the 76 years during which beneﬁcial organisms in the Mediterranean region of Europe. As a result, have been released for the biological control of weeds agents best adapted for California may not be avail- in California, complete control has been obtained for able. In addition, many of the California weed targets four weeds, H. perforatum, the Opuntia spp. on Santa also occur in other areas of the USA and Canada, areas Cruz Island, J. vulgaris, and C. virgata subsp. which generally have more mesic and temperate squarrosa (a transfer experiment), and substantial climates. During the initial efforts to introduce a new control has been achieved for an additional ﬁve agent to North America, researchers attempt to match species, T. terrestris, C. nutans, C. juncea, L. the climate of the area of origin with the initial area of salicaria, and S. molesta. For each of these projects, introduction. Once established, agents are collected the amount of herbicide applied and the costs for and shipped to other states including California. For control have been substantially reduced, and the level example, all of the agents released in California on of control provided by the biological control agents Centaurea diffusa Lam. (Asteraceae) and Centaurea has been maintained to date. DeBach (1964) reported stoebe L. (Asteraceae) were ﬁrst established in Mean Impact score (+SE) Mean Impact Score (+SE) Weed biological control in California, USA: review of the past 357 Table 2 Proportion of target weeds under various levels of biological control and overall establishment rate of species introduced as biological control agents reported by country or region (California, Hawaii, USA) Country/ Level of control Number of weed Agent establishment rate References region targets (%) Negligible ? partial Substantial Complete (%) (%) (%) Australia 20 0 80 15 69 1, 2 New Zealand 11 56 33 9 85 3, 4 South Africa 17 57 26 23 71 2, 5 Hawaii 48 14 38 21 61 6 California 58 26 16 19 82 7 1 Briese (2000), 2 McFadyen (2000), 3 Fowler et al. (2000), 4 Hayes et al. (2013), 5 Klein (2011), 6 Markin et al. (1992), 7 This report Montana, an area much colder and more temperate A third explanation for the low success rate in than California. Another example is the suite of agents California is that too little information is available to released on Eichhornia crassipes (Mart.) Solms make an accurate assessment of impact for some of the (Pontederiaceae) which were ﬁrst released in the established agents despite their presence here for southeastern USA, an area with a much more humid many years. For example, Hylobius transversovittatus climate than in California. Having a poor climate (Goeze) (Coleoptera: Curculionidae), a weevil that match with California may impede the ability of an feeds in the roots of L. salicaria, was released at agent to increase to population densities sufﬁcient to several ﬁeld sites in California from 1996 through provide successful control. 2001. Field samples at two release sites in 2002 (the A second explanation for the low rate of success of ﬁrst year following cessation of releases) showed H. weed biological control in California may be a lack of transfersovittatus to be present in four of ten plants sufﬁcient funding to support a project from beginning and two of ten plants, respectively (Villegas 2003). to end. Economically, it makes sense to share research Unfortunately, there has been no additional monitor- costs among states infested by a targeted weed. Also, it ing of this agent since then. Similarly, the level of makes sense to try agents established in other states control for some weeds, especially those identiﬁed as ﬁrst and, if not successful, then search for an agent that under partial control, may improve with time or with may perform better in California. However, taking the better quantitative information on the impact of the next step and pursuing a better agent may be delayed introduced agents. For example, Coombs et al. (2007) or eliminated altogether by the amount of funding reported that Salvia aethiopis L. (Lamiaceae) is under available. Low funding may have also interrupted good control in the sagebrush steppe communities in some of the older projects currently assessed as partial southeastern Oregon, USA. South of the state border in or negligible successes. Stakeholders and funding northeastern California, the results are less clear. In the agencies like to fund the newest, worst weed and when absence of good quantitative data on host and agent something new comes along, project funding can get abundance, the biological control of S. aethiopis is re-directed to the new target. It should be noted that, reported under partial control from discussions with while the number of scientists devoted classical weed local land managers who report no change in their biocontrol in the western USA had declined during the control efforts toward this species. One beneﬁt of this last ten years, more recently the number of weed retrospective analysis is to identify those weed biocontrol scientists in California has increased (Paul projects for which more information is necessary to Pratt, USDA-ARS Exotic and Invasive Weed better understand the system. It is important to keep in Research Unit, personal communication). As a result, mind that the information provided in this review is a snapshot in time and that it would be beneﬁcial to re- several of the older projects, E. crassipes, S. tragus, C. scoparius, C. solstitialis, and U. europaeus, are now assess these projects in the future. subjects of renewed research efforts. 123 358 M. J. Pitcairn Hatcher PE, Hinz HL, Rector BG (eds) Proceedings of the Biological control researchers have addressed only XII international symposium on biological control of a handful of the many exotic invasive weeds that infest weeds, pp 521–527 California. Biological control remains the most cost- Crawley MJ (1989) The successes and failures of weed bio- effective and environmentally-benign method of weed control using insects. Biocontrol News Inf 10(3):213–223 DeBach P (1964) The scope of biological control. In: DeBach P control and pressure to reduce herbicide use will (ed) Biological control of insect pests and weeds. Reinhold reinforce its use. The last 76 years have produced nine Publishing Co., New York, pp 3–20 successful projects. The establishment rate for new Denoth M, Frid L, Myers JH (2002) Multiple agents in biolog- biological control agents for the last 20 years is very ical control: improving the odds? Biol Control 24:20–30 Dunkle RL (1975) 1975 Annual report, biological control ser- high. Future research efforts that emphasize the vices project. California Department of Food and Agri- release of agents with a good potential for high impact culture, Sacramento on their host may increase the rate of project success Dunkle RL (1977) 1977 Annual report, biological control ser- and support further development of this critical weed vices project. California Department of Food and Agri- culture, Sacramento control method. Fowler SV, Syrett P, Hill RL (2000) Success and safety in the biological control environmental weeds in New Zealand. Acknowledgements The author thanks Ray Carruthers and Austral Ecol 25:553–562 John Herr for access to the release records at the USDA-ARS Gaskin JF, Schaal BA (2003) Molecular phylogenetic investi- Quarantine Facility at Albany, California; Rachel Winston for gation of US invasive Tamarix. Syst Bot 28(1):86–95 help in tracking down some of the old literature on agents Goeden RD, Fleschner CA, Ricker DW (1967) Biological released in California; and Nick Mills for comments on an early control of prickly pear cacti on Santa Cruz Island, Cali- draft of this manuscript. Lastly, great appreciation is extended to fornia. Hilgardia 38(16):579–606 Don Joley, Baldo Villegas, and Dale Woods for their tireless Harrison SP (2013) Plant and animal endemism in California. work in the introduction and release of beneﬁcial agents for University of California Press, Berkeley weed biological control in California. Hayes L, Fowler SV, Paynter Q, Groenteman R, Peterson P, Dodd S, Bellgard S (2013) Biocontrol of weeds: achieve- Open Access This article is distributed under the terms of the ments to date and future outlook. In: Dymond JR (ed) Creative Commons Attribution 4.0 International License (http:// Ecosystem services in New Zealand—conditions and creativecommons.org/licenses/by/4.0/), which permits unrest- trends. Manaaki Whenua Press, Lincoln, pp 375–385 ricted use, distribution, and reproduction in any medium, pro- Hoffmann JH (1995) Biological control of weeds: the way vided you give appropriate credit to the original author(s) and forward, a South African perspective. In: BCPC sympo- the source, provide a link to the Creative Commons license, and sium proceedings No 64: weeds in a changing world, indicate if changes were made. pp 77–89 Holloway JK (1964) Projects in biological control of weeds. In: DeBach P (ed) Biological control of insect pests and weeds. Chapman and Hall, London, pp 650–670 Huffaker CB, Kennett CE (1959) A ten-year study of vegeta- References tional changes associated with biological control of Kla- math weed. J Range Manag 12(2):69–82 Bakker ES (1971) An island called California. University of Klein H (2011) A catalogue of the insects, mites and pathogens California Press, Berkeley that have been used or rejected, or are under consideration, Briese DT (2000) Classical biological control. In: Sindel BM for the biological control of invasive alien plants in South (ed) Australian weed management systems. R.G. and F.J. Africa. Afr Entomol 19(2):515–549 Richardson Publishers, Melbourne, pp 161–192 Markin GP, Lai PY, Funasaki GY (1992) Status of biological Burdon JJ, Marshall DR (1981) Biological control and the control of weeds in Hawai’i and implications for managing reproductive mode of weeds. J Appl Ecol 18:649–658 native ecosystems. In: Stone CP, Smith CW, Tunison JT Chaboudez P, Sheppard AW (1995) Are particular weeds more (eds) Alien plant invasions in native ecosystems of Hawaii: amenable to biological control?—a reanalysis of mode of management and research. Cooperative National Park reproduction and life history. In: Delfosse ES, Scott RR Resources Studies Unit, University of Hawaii, Manoa, (eds) Proceedings of the VIII international symposium on pp 466–482 biological control of weeds, pp 95–102 McFadyen REC (2000) Successes in biological control of Coombs EM, Radtke H, Isaacson DL, Snyder SP (1996) Eco- weeds. In: Spencer NR (ed) Proceedings of the X interna- nomic and regional beneﬁts from the biological control of tional symposium on biological control of weeds, pp 3–14 tansy ragwort, Senecio jacobaea, in Oregon. In: Moran VC, Nechols JR (1995) Biological control in the western United Hoffmann JH (eds) Proceedings of the IX international States. University of California, Division of Agriculture symposium on biological control of weeds, pp 489–494 and Natural Resources, Oakland, CA, Publication 3361 Coombs EM, Miller JC, Andres LA, Turner CE (2007) Bio- Pemberton RW, Turner CE (1990) Biological control Senecio logical control of Mediterranean sage (Salvia aethiopis)in jacobaea in northern California, an enduring success. Oregon. In: Julien MH, Sforza R, Bon MC, Evans HC, Entomophaga 35(1):71–77 123 Weed biological control in California, USA: review of the past 359 Pitcairn MJ (2011) Biological control, of plants. In: Simberloff Villegas B (2003) Progress on the biological control program D, Rejmanek M (eds) Encyclopedia of biological inva- against purple loosestrife. In: Woods DM (ed) Biological sions. University of California Press, Berkeley, pp 63–70 control program annual summary, 2002. California Straw NA, Sheppard AW (1995) The role of plant dispersion Department of Food and Agriculture, Plant Health and Pest pattern in the success and failure of biological control. In: Prevention Services, Sacramento, p 38 Delfosse ES, Scott RR (eds) Proceedings of the VIII Winston RL, Schwarzlander M, Hinz HL, Day MD, Cock MJW, international symposium on biological control of weeds, Julien MH (2014) Biological control of weeds—a world th pp 161–168 catalogue of agents and their target weeds, 5 Edn. USDA Supkoff DM, Joley DB, Marois JJ (1988) Effect of introduced Forest Service, Forest Health Technology Enterprise biological control organisms on the density of Chondrilla Team, Morgantown, West Virginia, USA, FHTET-2014- juncea in California. J Appl Ecol 25(3):1089–1095 04 Takhtajan A (1986) Floristic regions of the world. University of Woods DM, Villegas B (2006) Biological control of squarrose California Press, Berkeley knapweed in northern California: a developing success Turner CE (1992) Biological approaches to weed management. story? In: Hoddle MS, Johnson MW (eds) Proceedings of th In: Beall T (ed) Beyond pesticides: biological approaches the 5 California conference on biological control, to pest management in California. University of California, Riverside, CA, pp. 66–70 Division of Agriculture and Natural Resources, Publication Number 21512, pp 32–67 Michael J. Pitcairn is a scientist with the California Depart- Villegas B (1998) Implementation status of biological control of ment of Food and Agriculture working on the classical weeds in California. In: Woods DM (ed) Biological control biological control of invasive weeds. program annual summary, 1997. California Department of Food and Agriculture, Plant Health and Pest Prevention Services, Sacramento, pp 35–38 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BioControl Springer Journals http://www.deepdyve.com/lp/springer-journals/weed-biological-control-in-california-usa-review-of-the-past-and-2RRbgeq7TU

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Publisher: Springer Journals
Copyright: Copyright © 2018 by The Author(s)
Subject: Life Sciences; Entomology; Plant Pathology; Agriculture; Animal Ecology; Animal Biochemistry; Behavioral Sciences
ISSN: 1386-6141
eISSN: 1573-8248
DOI: 10.1007/s10526-018-9884-6
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Abstract

BioControl (2018) 63:349–359 https://doi.org/10.1007/s10526-018-9884-6 Weed biological control in California, USA: review of the past and prospects for the future Michael J. Pitcairn Received: 31 March 2017 / Accepted: 23 April 2018 / Published online: 5 May 2018 The Author(s) 2018 Abstract Weed biological control in California, established, 12 species failed to establish, six species USA began in 1940 with the release of a native scale had their release sites destroyed, and ﬁve species are insect on native Opuntia spp. on Santa Cruz Island, too early to determine. Establishment rate was 82% just offshore from mainland California. Since then, a but the rate differed among taxonomic orders. Indi- total 39 weed species have been targets of biological vidual agents were scored according to level of impact control releases in California. Releases on 11 weed on their host and Coleoptera obtained the highest targets were transfer experiments where agents from average impact score and Diptera the lowest. Mean related weed hosts were released on a new host. Most impact scores over time showed a substantial drop in of the transfer experiment introductions failed but one the 1980s but later increased. Future research efforts weed was successfully controlled. Of the other 28 that emphasize introduction of high impact agents will weeds, release sites for three species were destroyed further support development of this critical weed and for six species releases are too recent to score, but control method for California. for 19 weeds, their level of control was rated as: complete control (three species), substantial control Keywords Weed Biological control California (ﬁve species), and partial (six species), and negligible Establishment rate Success rate control (ﬁve species). Overall, 42% of the projects provide successful control, a result lower than observed in other countries worldwide. Since 1940, 77 species of agents have been released: 54 species Introduction In April 1940, Harry S. Smith, a professor of Handling Editors: Mark Schwarzla¨nder, Cliff Moran and Entomology at the University of California in River- S. Raghu. side, collected crawlers of native Dactylopius tomen- Electronic supplementary material The online version of tosus (Lam.) (Hemiptera: Dactylopiidae) from local this article (https://doi.org/10.1007/s10526-018-9884-6) con- Opuntia spp. near the City of Riverside in southern tains supplementary material, which is available to authorized California, USA carried the live material by boat to users. Santa Cruz Island, located approximately 32 km M. J. Pitcairn (&) offshore from Santa Barbara County, and liberated California Department of Food and Agriculture, them onto two native Opuntia (O. littoralis (Engelm.) Biological Control Program, 3294 Meadowview Road, Cockerell and O. oricola Philbrick (Cactaceae)) Sacramento, CA 95832, USA (Goeden et al. 1967). This action was the ﬁrst use of e-mail: mike.pitcairn@cdfa.ca.gov 123 350 M. J. Pitcairn a live organism to control a weed in North America. Turner (1992), Nechols (1995) and Villegas (1998). Five years later, the leaf beetle, Chrysolina hyperici Details for other projects were obtained in the Annual (Forster) (Coleoptera: Chrysomelidae), was released Reports of the California Department of Food and on Hypericum perforatum L. (Hypericaceae), an Agriculture’s Biological Control Program and in exotic forb that had invaded the pastures and grazing unpublished records at the USDA Agricultural lands in northern California (Holloway 1964). This Research Service’s Quarantine Facility in Albany, second action was the ﬁrst use of an exotic organism to California and the Quarantine Facility at the Univer- control an exotic weed in North America. Since 1940, sity of California, Berkeley. The scientiﬁc names and 77 species of biological control organisms have been taxonomic classiﬁcations of the agents and their weed released on 39 weed species in California. The level of targets were updated and aligned with Winston et al. control that resulted from some of these releases has (2014). The information was entered into two Micro- been spectacular, such as the reduction of H. perfo- soft Excel (version 2013) spreadsheets, one with ratum (Huffaker and Kennett 1959) following the details on the weed targets (Supplementary Table S1) release of the two Chrysolina leaf beetles. Other and one with details on the individual agent species projects have failed to result in any meaningful level (Supplementary Table S2). Summary statistics were of control. generated using the functions of the spreadsheet. In Classical biological control is a weed control generating these two tables, the following deﬁnitions were used. method where host-speciﬁc natural enemies of a weed are introduced from its area of origin to its new area of infestation (Pitcairn 2011). For exotic weeds, this Target weed species involves the introduction of natural enemies of exotic origin. The intention is for the introduced natural For most projects, only one taxonomic entity was enemy to establish, increase in abundance, and, when identiﬁed for each target weed. There are three successful, cause enough feeding damage to substan- exceptions: (1) the three Opuntia taxa, O. littoralis, tially reduce reproduction and recruitment of its host O. oricola, and a hybrid of the two, on Santa Cruz plant. The regional decline of the targeted weed can be Island; (2) Tamarix spp. which, in California, consists dramatic and provides an impressive example of of three species: T. chinensis Lour., T. parviﬂora DC., invertebrate consumers controlling a plant’s abun- and T. ramosissima Ledeb. (Tamaricaceae) as well as dance. This paper describes an attempt to compile a hybrid combinations of all three (Gaskin and Schaal complete list of weed biological control projects in 2003); (3) Centaurea jacea L. (Asteraceae) which California from 1940 through 2015. This review is the consists of three sub-species: C. jacea subsp. jacea, C. ﬁrst comprehensive record of weed biological control jacea subsp. nigra (L.) Bonnier & Layens, and C. research in California and, for some projects, it is the jacea nothosubsp. pratensis (W.D.J. Koch) Celak. For ﬁrst published record. The information obtained on the this analysis, all related taxa within each exception are introduction and establishment of biological control counted as one target weed entity. agents is summarized and an assessment of the success in reducing the abundance of the weed target and the Biological control agent species level of control provided by the established agents is reported. For all agents, only species were counted, different biotypes or other taxonomic entities were not counted separately. For example, two biotypes of Coleophora Materials and methods parthenica Meyrick (Lepidoptera: Coleophoridae) were released against Halogeton glomeratus A list of target weeds and the beneﬁcial organisms (M.Bieb.) C.A. May (Chenopodiaceae): one collected released in California as biological control agents was from Salsola tragus L. (Chenopodiaceae) and another compiled by examining published, peer-reviewed collected from H. glomeratus. For this review, the literature as well as unpublished technical reports release of the two C. parthenica biotypes on H. and quarantine records. Some of the releases associ- glomeratus is counted as one agent-target ated with projects prior to 1990 were summarized in combination. 123 Weed biological control in California, USA: review of the past 351 Number of introductions tragus biotype occurred in 1974 and 1975 (Dunkle 1975) and in 1976, a single release of the H. The number of introductions is the unique combina- glomeratus biotype occurred (Dunkle 1977). The tion of an agent and a target weed. Some agents were focus of the research effort at that time was S. tragus used on more than one weed target and are counted as and the release of the H. glomeratus biotype was a separate introductions. For example, Rhinocyllus one-time event, so, for this analysis, the H. glomeratus conicus (Fro¨lich) (Coleoptera: Curculionidae) was project is considered to be a transfer experiment. introduced on Carduus nutans L. (Asteraceae), Car- duus pycnocephalus L. (Asteraceae), Onopordum Measures of success, weeds acanthium L. (Asteraceae), and Silybum marianum (L.) Gaertn. (Asteraceae). Each of these were counted A common problem in attempting to review the as separate agent-target introductions. success of weed biological control projects worldwide is the lack of quantitative information on the amount Date of introduction of reduction in the target weed (Crawley 1989; Hoffmann 1995; MacFadyen 2000). California has The year of the ﬁrst release of an agent is the year for the same lack of quantitative control information. which a project began. Only a handful of projects, H. perforatum (Huffaker and Kennett 1959), Jacobae vulgaris Gaertn. (Aster- Classical biological control projects and transfer aceae) (Pemberton and Turner 1990), and Chondrilla experiments juncea L. (Asteraceae) (Supkoff et al. 1988) have quantitative before-and-after data on the population A classical biological control project typically consists abundance of the target weed in California. While of ﬁve steps: (1) identiﬁcation of the target weed, (2) these studies are decades old, the lack of resurgence of foreign exploration, (3) host speciﬁcity testing, (4) these weeds does suggest that the results reported may release from quarantine (initial establishment), and (5) still have some relevance. post-release monitoring and redistribution. Ideally, the Hoffmann (1995) proposed three qualitative cate- biological control agent is obtained from the target gories of project success for weed biological control weed in its area of origin and released on the same projects in South Africa: Complete control—when target species in the area of introduction. In some attempts at control are no longer needed in areas where cases, agents from one weed are released on another the agents have established, Substantial control— closely-related weed species to see if the agent where other control efforts are reduced but still provides some beneﬁts. This is particularly true for required to reduce the target weed to acceptable levels agents that have been approved for introduction and over the whole region infested, and Negligible there are other noxious weed species closely related to control—where there has been little or no reduction the target weed in the invaded region. For these in weed abundance or the need to control it. For the projects, the related weed species was not examined in current analysis, a fourth category is added, Partial its area of origin and the released agents were not control—where there is some evidence of decline in obtained from the new target and thereby lack any weed abundance in a limited portion of its infested evolutionary connection and are considered to be range or in some habitats but other control efforts ‘‘transfer experiments.’’ For example, R. conicus was continue with little reduction in use. This last category collected from C. nutans in Italy and released on C. is one level up from Negligible control but below nutans in California where it established. Later, R. Substantial control. It has been included in other conicus weevils were collected from C. nutans in retrospective analyses (Burdon and Marshall 1981; California and released on O. acanthium in California Denoth et al. 2002) and is useful in identifying projects where it failed to establish. The latter introduction is that may have received some beneﬁt from the identiﬁed as a transfer experiment. There is one introduction of biological control agents but the exception: two biotypes of C. parthenica were amount of reduction has not been sufﬁcient to reduce released on H. glomeratus, one reared from S. tragus control efforts by land managers and stakeholders. The and one reared from H. glomeratus. Releases of the S. success ratings are reported as follows: Complete 123 352 M. J. Pitcairn California as an ecoregion control, 3; Substantial control, 2; Partial control, 1; Negligible control, 0. The state of California is one of 48 contiguous states Measures of success, agents that make up the United States of America in the central portion of North American continent. The state The impact of a biological control agent on popula- is located along the western edge of the continent with the Paciﬁc Ocean as its western border. Despite tions of its host plant is dependent on three factors: amount of damage caused by an individual or popu- California being a part of a larger landmass, its unique lation unit of an agent, the local abundance of agents geography (ocean on the west, Sierra Nevada Moun- per individual host plant, and the regional occurrence tains along the eastern border, the Klamath and of the agent over the area infested by the target weed. Cascade Mountains in the north and the Mojave and Sonoran deserts in the southwest) has isolated much of The most successful agents are those that build up large populations on their host plant and inﬂict California from the rest of the continent. For many plant and animal species, these natural geographic sufﬁcient damage to cause a reduction in host abun- dance. Agents that remain scarce in relation to the barriers have limited long-distance colonization and gene ﬂow from close relatives in neighboring areas abundance of their host are unlikely to cause a meaningful reduction in the abundance of their target and this isolation has resulted in a high level of endemism. For example, 57 species of conifers occur weed. Here, an assessment of the level of control (impact) provided by each of the established agents is in California, 27 species are endemic and occur reported. Impact scores for each agent are based on nowhere else in North America or the world (Bakker Klein (2011) and modiﬁed as follows: Trivial: estab- 1971). Overall, it is estimated that 35% of plant lished but remained low in abundance, throughout the species native to California are endemic (Harrison 2013). range of its host, Moderate: obtained a moderate level of abundance in a limited area of its host but was low The climate dominating most of California is Mediterranean, a climate that is rare worldwide and in abundance or absent elsewhere, Considerable: obtained moderate to high levels of abundance in part occurs in only ﬁve other locations: Chile, South Africa, two locations in Australia, and southern or all of the infested range but, alone, was not able to reduce host abundance, Extensive: obtained moderate Europe. Mediterranean climate has cool, wet winters to high levels of abundance that resulted in successful and hot, dry summers. This unusual climate is further control of its host plant, and Unknown: not enough complicated by the extreme length of the summer information is available to make a reasonable decision drought, which lasts longer in California than else- regarding impact or their release occurred too where, and by the unusually high summer tempera- recently. Agent impact is reported as follows: Trivial, tures. During summer, daytime high temperatures commonly exceed 35 C and daytime RH drops below 1; Moderate, 2; Considerable, 3; Extensive, 4; Unknown, U. 10%. Botanists have divided the world landmass into Statistics ﬂoristic regions based on the local level of endemism within the dominant plant communities and the Rates of establishment and impact scores are summa- possibility of shared evolutionary histories of the rized only for those target weeds or agents for which constituent species (Takhtajan 1986). Some regions information is available. For some established agents, are further divided into ﬂoristic provinces and phyto- little or no follow-up has been performed and their geographers have identiﬁed the California ﬂoristic level of control is unknown. In calculating average province as a distinct area separated from other areas rates and scores, information from species with in North America (Takhtajan 1986). As much as 70% of the California Floristic Province is included in the unknown status are not included. political boundary of the state of California (Harrison 2013). It is reasonable, then, to consider California its own ecoregion and that the performance of agents and 123 Weed biological control in California, USA: review of the past 353 Measures of success, weeds the number of successful control projects may not be similar with other areas of North America. Of the 39 weed targets on which biological control agents were intentionally released, 11 were identiﬁed as transfer experiments where agents were obtained Results from closely-related exotic weeds (Supplementary Table S1). Most of the transfer experiment introduc- From 1940 through 2015, 77 species of biological control agents were released on 39 weed targets in tions failed (establishment rate = 32%, 7/(24-2 California (Supplementary Tables S1 and S2). Some unknowns)). However, the releases on C. virgata agents were released on more than one target weed subsp. squarrosa were very successful, where ﬁve of (e.g., R. conicus was released on four target weeds) so, seven agents established and two agents, Larinus minutus Gyllenhal (Coleoptera: Curculionidae) and in total, 101 unique target-agent introductions occurred during this time period. The weed targets Bangasternus fausti (Reitter) (Coleoptera: Curculion- idae), built up high numbers and resulted in a 99% include taxa from 18 families and 12 orders. The family Asteraceae was the most represented with 16 reduction in seed production effectively stopping all plant recruitment (Woods and Villegas 2006). In the species, followed by Euphorbiaceae (three species), Chenopodiaceae (two species), Fabaceae (two spe- years following, adult plants have slowly died from other causes and now C. virgata subsp. squarrosa is cies) and Hypericaceae (two species). The other 13 families (Amaranthaceae, Araceae, Brassicaceae, greatly reduced in abundance and no longer consid- Cactaceae, Hydrocharitaceae, Lamiaceae, Lythraceae, ered an economic weed (Woods and Villegas 2006). In Plantaginaceae, Poaceae, Pontederiaceae, Salvini- evaluating the success of the classical weed biocontrol aceae, Tamaricaceae, Zygophyllaceae) were repre- projects, the 11 weed targets involved in the transfer experiments were removed from consideration. sented with one species each. All plant life histories are represented with perennial species the most In total, 28 weeds have been classical weed biological control targets (Table 1). For nine of these abundant (22 species), followed by biennial (ten species) and annual (seven species). The most com- targets, success was not evaluated. Three projects, Alternanthera philoxeriodes (Mart.) Griseb. (Amaran- mon plant growth form was herbaceous forbs (33 species), followed by shrubs (three species), one grass thaceae), Hydrilla verticillata (L. f.) Royle (Hy- (Arundo donax L. (Poaceae)), one tree (Tamarix spp. drocharitaceae), and Pistia stratoites L. (Araceae) complex) and one target of succulents (Opuntia spp. had each of their study locations destroyed shortly on Santa Cruz Island). The targeted weed species after release of their agents. There are six projects for occurred in a variety of habitats, with rangelands (30 which releases occurred within the last ten years and species) and natural areas (24 species) the most not enough time has elapsed to allow evaluation. A total of 19 weeds are considered further and the level common, followed by aquatic habitats (includes riparian species and free-ﬂoating aquatic macro- of control achieved for each project shows the following results (Table 1): ﬁve weeds showed neg- phytes) (eight species) and managed pastures and cultivated lands (eight species) (the total exceeds 39 ligible control, six weeds are rated as partial control, ﬁve weeds are under substantial control, and three species because some weeds occur in multiple habi- tats). The number of agents released on an individual weeds are under complete control (H. perforatum, the Opuntia spp. on Santa Cruz Island, and J. vulgaris). targeted weed species ranged from one to seven agents, with the Opuntia spp. on Santa Cruz Island, The ﬁve weeds under substantial control (Tribulus Centaurea solstitialis L. (Asteraceae), and Centaurea terrestris L. (Zygophyllaceae), C. nutans, C. juncea, virgata Lam. subsp. squarrosa (Boiss.) Gugler (Aster- Lythrum salicaria L. (Lythraceae), and Salvinia aceae), each receiving the highest number of agents. molesta D.S. Mitch. (Salviniaceae)) are under com- plete control in some areas of their range, but much The rate of agent establishment by weed target ranged from 0 to 100%. However the majority of targets less or little control occurs in other areas of their infestation. For example, L. salicaria is under com- showed intermediate rates of establishment. plete control in area of Big Lake and along the Fall River in eastern Shasta County, an area at 41 latitude 123 354 M. J. Pitcairn Table 1 List classical weed biological control targets in California from 1940 to 2015 Scientiﬁc name Common name Year of 1st Level of Number of Agents introduction control RE C2 C3 Ulex europaeus L. Gorse 1953 0 2 2 1 0 Cytisus scoparius (L.) Link Scotch Broom 1960 0 2 2 1 0 Silybum marianum (L.) Gaertn. Milk Thistle 1969 0 1 1 1 0 Salsola tragus L. Russian Thistle 1973 0 2 2 0 0 Eichhornia crassipes (Mart.) Solms Water Hyacinth 1982 0 4 3 1 0 Centaurea solstitialis L. Yellow Starthistle 1969 1 7 6 1 0 Carduus pycnocephalus L. Italian Thistle 1973 1 1 1 1 0 Centaurea diffusa Lam. Diffuse Knapweed 1976 1 4 4 3 0 ? 2U Salvia aethiopis L. Mediterranean Sage 1976 1 1 1 1 0 ? 1U Centaurea stoebe L. Spotted Knapweed 1993 1 5 5 1 ? 1U 0 Cirsium vulgare (Savi.) Ten. Bull Thistle 1993 1 1 1 1 0 Tribulus terrestris L. Puncturevine 1961 2 2 2 2 2 Carduus nutans L. Musk Thistle 1974 2 1 1 1 1 Chondrilla juncea L. Skeletonweed 1975 2 4 3 ? 1U 2 1 Lythrum salicaria L. Purple Loosestrife 1996 2 4 4 1 ? 3U 1 Salvinia molesta D.S. Mitch. Giant Salvinia 2002 2 1 1 1 1 Opuntia spp. Prickly Pear Cactus 1940 3 7 3 2 1 Hypericum perforatum L. Klamath Weed 1945 3 6 5 2 2 Jacobaea vulgaris Gaertn. Tansy Ragwort 1959 3 3 2 2 2 Cirsium arvense (L.) Scop. Canada Thistle 1966 TE 3 2 0 0 Euphorbia esula L. Leafy Spurge 2001 TE 3 2 0 ? 1U 0 Tamarix spp. Saltcedar 2001 TE 2 1 ? 1U 1 0 ? 1U Linaria dalmatica ssp. dalmatica (L.) Mill. Dalmatian Toadﬂax 2008 TE 1 1 1 0 ? 1U Arundo donax L. Giant Reed 2010 TE 2 1 ? 1U 0 ? 1U 0 Rhaponticum repens (L.) Hidalgo Russian Knapweed 2011 TE 2 0 ? 1U 0 0 Alternanthera philoxeroides (Mart.) Griseb. Alligatorweed 1964 NA 3 Ex – – Hydrilla verticillata (L. f.) Royle Hydrilla 1991 NA 2 Ex – – Pistia stratiotes L. Waterlettuce 2013 NA 1 Ex – – Totals 77 56 ? 4U 27 ? 6U 11 ? 5U For each weed target, the current level of control and the number of agents released, established, and the level of agent impact are reported. Target weeds are listed by order of level of control and year of introduction of ﬁrst agent Opuntia littoralis (Engelm.) Cockerell, O. oricola Philbrick, and hybrids between these two species Tamarix chinensis Lour., T. parviﬂora DC., T. ramosissima Ledeb., and hybrids among these species Level of control of the target weed: 0 = negligible control; 1 = partial control; 2 = substantial control; 3 = complete control; TE = too early to rate; NA = no information available R number of agents released, E number of agents established; C 2 number of established agents with impact scores 2 and higher (from Supplementary Table S2), C 3 number of established agents with impact scores 3 and higher (from Supplementary Table S2), U status unknown, Ex agents extirpated in northern California. However, L. salicaria occurs in photoperiod limitations (unpublished data). The several locations further south in California, including beetles did establish in Butte County, a low elevation tributaries of the Feather River in Butte County, the (35 m) location approximately 80 km south of Big Kings River in Fresno County, and the Kern River in Lake, but the growing season begins before and Kern County. The two Galerucella beetles did not extends after the active period of the beetles, so the establish in areas of California south of 39 latitude plants are able to outgrow the damage (unpublished (e.g., Fresno and Kern counties) because of data). 123 Weed biological control in California, USA: review of the past 355 18 100 Combining the number of weed targets under substantial and complete control, the success rate is 42% (8/19 weed targets). Out of the 58 unique target- agent introductions associated with the 19 classical 60 biological control target weeds (Table 1), 86% of these introductions resulted in establishment of the agent (49/(58-1 unknown)). Each of the 19 target 4 weeds had at least one agent established. When weed 10 0 0 targets are sorted by life history, annual weeds have a lower rate of success (20% of targets under complete or substantial control) compared to the biennial (60%) and perennial (44%) weed targets, a result similar to Number Released % Establishment that reported by Chaboudez and Sheppard (1995) and Fig. 1 Numbers of weed biological control agents released and Straw and Sheppard (1995). rates of establishment in California by decade Measures of success, agents For those agents for which information is available, an assessment of their impact on their host was A total of 77 species have been released as weed recorded (Supplementary Table S2). Two associations biological control agents from 1940 through 2015 are of interest. First, the average impact score by order (Supplementary Table S2). Most species were insects shows the Coleoptera to have the highest average (n = 72) but two mite and three fungal species were score and the Diptera to have the lowest average score also released. Species of Coleoptera were the most (Fig. 2a). Second, the average impact score of agents represented (n = 37), followed by Diptera (n = 13) released varied by decade (Fig. 2b). Interestingly, the and Lepidoptera (n = 12). By family, Curculionidae average impact score showed a substantial drop in the and Chrysomelidae were the most used (n = 17 and 1970s and 1980s, suggesting that, for the agents 12, respectively), followed by Tephritidae (n = 8). All released during this time period, little beneﬁt appears other taxonomic families had four or less species to have come from their presence. introduced. Overall, the establishment rate for agents The combined impact of the complex of agents that on at least one target weed was 82% (54/(77-11(5 established on each weed target was examined by unknowns and 6 extirpated))) but rate of establishment tallying the number of agents that resulted in impact differed among orders and families with the Acari scores of two or higher and the number of agents (two species), Hymenoptera (one species), and fungi having impact scores three or higher (Table 1). The (two species) having the highest rate of establishment results show that for the 28 classical biological control (100%), followed by Coleoptera (83%), Diptera targets 54% (27/(56-6 unknowns)) of established (69%), Hemiptera (67%), and Lepidoptera (55%). agents provided a moderate or higher level of impact The release rate averaged 9.7 species per decade with a on their hosts. Eleven agents are rated with impact lower release rate initially and a notable drop in the scores of three or higher, indicating that 24% (11/(56- 1980s (Fig. 1). However, the rate of establishment 11 unknowns)) of the agents that established are across decades showed an increasing trend with the considered effective agents and contributed to suc- highest establishment rate (88%) obtained in the two cessful control of their hosts. In a review of interna- most recent full decades (1990–2009). Among the tional weed biological control projects, Crawley insect and mite biological control agents, 58% were (1989) reported an average of 25% of established concealed feeders/borers (including seed-feeding agents to be effective, suggesting that the results in insects), 20% were chewers, 14% were sap feeders, California are similar. and 8% were gallers. All plant parts were targeted by the agents with 37% being leaf-feeders, 26% seed/ ﬂower feeders, 22% feeding on roots and lower stems, and 15% feeding on the main/upper part of stems. Number of Agents Released % Establishment 356 M. J. Pitcairn 3.50 that the successful control of Klamath weed in California resulted in a cumulative savings of $14 3.00 million dollars during 1953 through 1959. In Oregon where J. vulgaris is also considered to be under 2.50 complete control, it was estimated that the project 2.00 resulted in an annual savings of more than ﬁve million dollars due to reduced losses to livestock, increased 1.50 productivity of pastures, and reduced herbicide use (Coombs et al. 1996). It is likely that California has 1.00 reaped similar amounts of economic and environmen- tal beneﬁts from each of these classical weed biolog- ical control programs. Despite these successes, there is much more to accomplish. A total of six weeds are considered under partial control and a further ﬁve weeds show little or 3.50 no control (Table 1). In comparison with weed 3.00 biological control programs in other countries, the rate of success for California programs (42%) is low 2.50 (Table 2). Classical weed biological control programs in Australia, New Zealand, and South Africa have 2.00 each achieved rates of success (substantial and com- 1.50 plete control combined) of over 80%. Interestingly, the rate of establishment of introduced agents and the 1.00 proportion of agents that are effective in California are 1940s 1950s 1960s 1970s 1980s 1990s 2000s (n=4) (n=5) (n=6) (n=7) (n=6) (n=9) (n=3) similar to that reported for Australia, New Zealand, and South Africa so the reason for the low success rate Fig. 2 a Average impact value (? SE) of weed biological in California may be due to other factors. Three control agents established in California by taxonomic order. possible explanations are considered. Sample size (number of species) is identiﬁed in the parentheses. Orders with only one species are not displayed. b Average The ﬁrst explanation is that, for many agents, there impact value (? SE) of weed biological control agents released is a mis-match with climate. The Mediterranean in California by decade. Sample size (number of species) is climate which dominates California is unusual world- identiﬁed in the parentheses. Values are calculated from wide and the lack of agents sourced from a Mediter- individual agent data in Supplementary Table S2 ranean region may contribute to the low success rate and the low impact scores for agents that establish. Discussion While many of the weeds targeted for control in California are of European origin, not all weeds occur In the 76 years during which beneﬁcial organisms in the Mediterranean region of Europe. As a result, have been released for the biological control of weeds agents best adapted for California may not be avail- in California, complete control has been obtained for able. In addition, many of the California weed targets four weeds, H. perforatum, the Opuntia spp. on Santa also occur in other areas of the USA and Canada, areas Cruz Island, J. vulgaris, and C. virgata subsp. which generally have more mesic and temperate squarrosa (a transfer experiment), and substantial climates. During the initial efforts to introduce a new control has been achieved for an additional ﬁve agent to North America, researchers attempt to match species, T. terrestris, C. nutans, C. juncea, L. the climate of the area of origin with the initial area of salicaria, and S. molesta. For each of these projects, introduction. Once established, agents are collected the amount of herbicide applied and the costs for and shipped to other states including California. For control have been substantially reduced, and the level example, all of the agents released in California on of control provided by the biological control agents Centaurea diffusa Lam. (Asteraceae) and Centaurea has been maintained to date. DeBach (1964) reported stoebe L. (Asteraceae) were ﬁrst established in Mean Impact score (+SE) Mean Impact Score (+SE) Weed biological control in California, USA: review of the past 357 Table 2 Proportion of target weeds under various levels of biological control and overall establishment rate of species introduced as biological control agents reported by country or region (California, Hawaii, USA) Country/ Level of control Number of weed Agent establishment rate References region targets (%) Negligible ? partial Substantial Complete (%) (%) (%) Australia 20 0 80 15 69 1, 2 New Zealand 11 56 33 9 85 3, 4 South Africa 17 57 26 23 71 2, 5 Hawaii 48 14 38 21 61 6 California 58 26 16 19 82 7 1 Briese (2000), 2 McFadyen (2000), 3 Fowler et al. (2000), 4 Hayes et al. (2013), 5 Klein (2011), 6 Markin et al. (1992), 7 This report Montana, an area much colder and more temperate A third explanation for the low success rate in than California. Another example is the suite of agents California is that too little information is available to released on Eichhornia crassipes (Mart.) Solms make an accurate assessment of impact for some of the (Pontederiaceae) which were ﬁrst released in the established agents despite their presence here for southeastern USA, an area with a much more humid many years. For example, Hylobius transversovittatus climate than in California. Having a poor climate (Goeze) (Coleoptera: Curculionidae), a weevil that match with California may impede the ability of an feeds in the roots of L. salicaria, was released at agent to increase to population densities sufﬁcient to several ﬁeld sites in California from 1996 through provide successful control. 2001. Field samples at two release sites in 2002 (the A second explanation for the low rate of success of ﬁrst year following cessation of releases) showed H. weed biological control in California may be a lack of transfersovittatus to be present in four of ten plants sufﬁcient funding to support a project from beginning and two of ten plants, respectively (Villegas 2003). to end. Economically, it makes sense to share research Unfortunately, there has been no additional monitor- costs among states infested by a targeted weed. Also, it ing of this agent since then. Similarly, the level of makes sense to try agents established in other states control for some weeds, especially those identiﬁed as ﬁrst and, if not successful, then search for an agent that under partial control, may improve with time or with may perform better in California. However, taking the better quantitative information on the impact of the next step and pursuing a better agent may be delayed introduced agents. For example, Coombs et al. (2007) or eliminated altogether by the amount of funding reported that Salvia aethiopis L. (Lamiaceae) is under available. Low funding may have also interrupted good control in the sagebrush steppe communities in some of the older projects currently assessed as partial southeastern Oregon, USA. South of the state border in or negligible successes. Stakeholders and funding northeastern California, the results are less clear. In the agencies like to fund the newest, worst weed and when absence of good quantitative data on host and agent something new comes along, project funding can get abundance, the biological control of S. aethiopis is re-directed to the new target. It should be noted that, reported under partial control from discussions with while the number of scientists devoted classical weed local land managers who report no change in their biocontrol in the western USA had declined during the control efforts toward this species. One beneﬁt of this last ten years, more recently the number of weed retrospective analysis is to identify those weed biocontrol scientists in California has increased (Paul projects for which more information is necessary to Pratt, USDA-ARS Exotic and Invasive Weed better understand the system. It is important to keep in Research Unit, personal communication). As a result, mind that the information provided in this review is a snapshot in time and that it would be beneﬁcial to re- several of the older projects, E. crassipes, S. tragus, C. scoparius, C. solstitialis, and U. europaeus, are now assess these projects in the future. subjects of renewed research efforts. 123 358 M. J. Pitcairn Hatcher PE, Hinz HL, Rector BG (eds) Proceedings of the Biological control researchers have addressed only XII international symposium on biological control of a handful of the many exotic invasive weeds that infest weeds, pp 521–527 California. Biological control remains the most cost- Crawley MJ (1989) The successes and failures of weed bio- effective and environmentally-benign method of weed control using insects. Biocontrol News Inf 10(3):213–223 DeBach P (1964) The scope of biological control. In: DeBach P control and pressure to reduce herbicide use will (ed) Biological control of insect pests and weeds. Reinhold reinforce its use. The last 76 years have produced nine Publishing Co., New York, pp 3–20 successful projects. The establishment rate for new Denoth M, Frid L, Myers JH (2002) Multiple agents in biolog- biological control agents for the last 20 years is very ical control: improving the odds? Biol Control 24:20–30 Dunkle RL (1975) 1975 Annual report, biological control ser- high. Future research efforts that emphasize the vices project. California Department of Food and Agri- release of agents with a good potential for high impact culture, Sacramento on their host may increase the rate of project success Dunkle RL (1977) 1977 Annual report, biological control ser- and support further development of this critical weed vices project. California Department of Food and Agri- culture, Sacramento control method. Fowler SV, Syrett P, Hill RL (2000) Success and safety in the biological control environmental weeds in New Zealand. Acknowledgements The author thanks Ray Carruthers and Austral Ecol 25:553–562 John Herr for access to the release records at the USDA-ARS Gaskin JF, Schaal BA (2003) Molecular phylogenetic investi- Quarantine Facility at Albany, California; Rachel Winston for gation of US invasive Tamarix. Syst Bot 28(1):86–95 help in tracking down some of the old literature on agents Goeden RD, Fleschner CA, Ricker DW (1967) Biological released in California; and Nick Mills for comments on an early control of prickly pear cacti on Santa Cruz Island, Cali- draft of this manuscript. Lastly, great appreciation is extended to fornia. Hilgardia 38(16):579–606 Don Joley, Baldo Villegas, and Dale Woods for their tireless Harrison SP (2013) Plant and animal endemism in California. work in the introduction and release of beneﬁcial agents for University of California Press, Berkeley weed biological control in California. Hayes L, Fowler SV, Paynter Q, Groenteman R, Peterson P, Dodd S, Bellgard S (2013) Biocontrol of weeds: achieve- Open Access This article is distributed under the terms of the ments to date and future outlook. In: Dymond JR (ed) Creative Commons Attribution 4.0 International License (http:// Ecosystem services in New Zealand—conditions and creativecommons.org/licenses/by/4.0/), which permits unrest- trends. Manaaki Whenua Press, Lincoln, pp 375–385 ricted use, distribution, and reproduction in any medium, pro- Hoffmann JH (1995) Biological control of weeds: the way vided you give appropriate credit to the original author(s) and forward, a South African perspective. In: BCPC sympo- the source, provide a link to the Creative Commons license, and sium proceedings No 64: weeds in a changing world, indicate if changes were made. pp 77–89 Holloway JK (1964) Projects in biological control of weeds. In: DeBach P (ed) Biological control of insect pests and weeds. Chapman and Hall, London, pp 650–670 Huffaker CB, Kennett CE (1959) A ten-year study of vegeta- References tional changes associated with biological control of Kla- math weed. J Range Manag 12(2):69–82 Bakker ES (1971) An island called California. University of Klein H (2011) A catalogue of the insects, mites and pathogens California Press, Berkeley that have been used or rejected, or are under consideration, Briese DT (2000) Classical biological control. In: Sindel BM for the biological control of invasive alien plants in South (ed) Australian weed management systems. R.G. and F.J. Africa. Afr Entomol 19(2):515–549 Richardson Publishers, Melbourne, pp 161–192 Markin GP, Lai PY, Funasaki GY (1992) Status of biological Burdon JJ, Marshall DR (1981) Biological control and the control of weeds in Hawai’i and implications for managing reproductive mode of weeds. J Appl Ecol 18:649–658 native ecosystems. In: Stone CP, Smith CW, Tunison JT Chaboudez P, Sheppard AW (1995) Are particular weeds more (eds) Alien plant invasions in native ecosystems of Hawaii: amenable to biological control?—a reanalysis of mode of management and research. Cooperative National Park reproduction and life history. In: Delfosse ES, Scott RR Resources Studies Unit, University of Hawaii, Manoa, (eds) Proceedings of the VIII international symposium on pp 466–482 biological control of weeds, pp 95–102 McFadyen REC (2000) Successes in biological control of Coombs EM, Radtke H, Isaacson DL, Snyder SP (1996) Eco- weeds. In: Spencer NR (ed) Proceedings of the X interna- nomic and regional beneﬁts from the biological control of tional symposium on biological control of weeds, pp 3–14 tansy ragwort, Senecio jacobaea, in Oregon. In: Moran VC, Nechols JR (1995) Biological control in the western United Hoffmann JH (eds) Proceedings of the IX international States. University of California, Division of Agriculture symposium on biological control of weeds, pp 489–494 and Natural Resources, Oakland, CA, Publication 3361 Coombs EM, Miller JC, Andres LA, Turner CE (2007) Bio- Pemberton RW, Turner CE (1990) Biological control Senecio logical control of Mediterranean sage (Salvia aethiopis)in jacobaea in northern California, an enduring success. Oregon. In: Julien MH, Sforza R, Bon MC, Evans HC, Entomophaga 35(1):71–77 123 Weed biological control in California, USA: review of the past 359 Pitcairn MJ (2011) Biological control, of plants. In: Simberloff Villegas B (2003) Progress on the biological control program D, Rejmanek M (eds) Encyclopedia of biological inva- against purple loosestrife. In: Woods DM (ed) Biological sions. University of California Press, Berkeley, pp 63–70 control program annual summary, 2002. California Straw NA, Sheppard AW (1995) The role of plant dispersion Department of Food and Agriculture, Plant Health and Pest pattern in the success and failure of biological control. In: Prevention Services, Sacramento, p 38 Delfosse ES, Scott RR (eds) Proceedings of the VIII Winston RL, Schwarzlander M, Hinz HL, Day MD, Cock MJW, international symposium on biological control of weeds, Julien MH (2014) Biological control of weeds—a world th pp 161–168 catalogue of agents and their target weeds, 5 Edn. USDA Supkoff DM, Joley DB, Marois JJ (1988) Effect of introduced Forest Service, Forest Health Technology Enterprise biological control organisms on the density of Chondrilla Team, Morgantown, West Virginia, USA, FHTET-2014- juncea in California. J Appl Ecol 25(3):1089–1095 04 Takhtajan A (1986) Floristic regions of the world. University of Woods DM, Villegas B (2006) Biological control of squarrose California Press, Berkeley knapweed in northern California: a developing success Turner CE (1992) Biological approaches to weed management. story? In: Hoddle MS, Johnson MW (eds) Proceedings of th In: Beall T (ed) Beyond pesticides: biological approaches the 5 California conference on biological control, to pest management in California. University of California, Riverside, CA, pp. 66–70 Division of Agriculture and Natural Resources, Publication Number 21512, pp 32–67 Michael J. Pitcairn is a scientist with the California Depart- Villegas B (1998) Implementation status of biological control of ment of Food and Agriculture working on the classical weeds in California. In: Woods DM (ed) Biological control biological control of invasive weeds. program annual summary, 1997. California Department of Food and Agriculture, Plant Health and Pest Prevention Services, Sacramento, pp 35–38

Journal

BioControl – Springer Journals

Published: May 5, 2018

References

An island called California

Bakker, ES
Australian weed management systems

Briese, DT
Biological control and the reproductive mode of weeds

Burdon, JJ; Marshall, DR
The successes and failures of weed biocontrol using insects

Crawley, MJ
Biological control of insect pests and weeds

DeBach, P
Multiple agents in biological control: improving the odds?

Denoth, M; Frid, L; Myers, JH
1975 Annual report, biological control services project

Dunkle, RL
1977 Annual report, biological control services project

Dunkle, RL
Success and safety in the biological control environmental weeds in New Zealand

Fowler, SV; Syrett, P; Hill, RL
Molecular phylogenetic investigation of US invasive Tamarix

Gaskin, JF; Schaal, BA
Biological control of prickly pear cacti on Santa Cruz Island, California

Goeden, RD; Fleschner, CA; Ricker, DW
Plant and animal endemism in California

Harrison, SP
Ecosystem services in New Zealand—conditions and trends

Hayes, L; Fowler, SV; Paynter, Q; Groenteman, R; Peterson, P; Dodd, S; Bellgard, S
Biological control of insect pests and weeds

Holloway, JK
A ten-year study of vegetational changes associated with biological control of Klamath weed

Huffaker, CB; Kennett, CE
A catalogue of the insects, mites and pathogens that have been used or rejected, or are under consideration, for the biological control of invasive alien plants in South Africa

Klein, H
Alien plant invasions in native ecosystems of Hawaii: management and research

Markin, GP; Lai, PY; Funasaki, GY
Biological control Senecio jacobaea in northern California, an enduring success

Pemberton, RW; Turner, CE
Encyclopedia of biological invasions

Pitcairn, MJ
Effect of introduced biological control organisms on the density of Chondrilla juncea in California

Supkoff, DM; Joley, DB; Marois, JJ
Floristic regions of the world

Takhtajan, A
Biological control program annual summary, 1997

Villegas, B
Biological control program annual summary, 2002

Villegas, B

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Weed biological control in California, USA: review of the past and prospects for the future

Weed biological control in California, USA: review of the past and prospects for the future

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Weed biological control in California, USA: review of the past and prospects for the future

Weed biological control in California, USA: review of the past and prospects for the future

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