BioControl (2018) 63:319–331 https://doi.org/10.1007/s10526-018-9890-8 REVIEW Biological control of weeds: an analysis of introductions, rates of establishment and estimates of success, worldwide . . . M. Schwarzlander Hariet L. Hinz R. L. Winston M. D. Day Received: 4 December 2017 / Accepted: 7 May 2018 / Published online: 31 May 2018 The Author(s) 2018 Abstract The foremost document that comprehen- 313 species, for which impact could be categorized, sively reports on biological control introductions 172 (55.0%) caused medium, variable or heavy levels against weeds—‘Biological control of weeds: a world of damage (impacts). Of all releases made through catalogue of agents and their target weeds’—has been 2012, 982 (63.2%) led to establishment. Forty-two updated and now includes all deliberate releases made releases were judged too early post-release to catego- through 2012. It includes data on 1555 intentional rize impact, leaving 940 releases for which impact releases of 468 biological control agent species used analyses were conducted. Similar to agent species, against 175 species of target weeds in 48 plant approximately half of the established releases (503 or families, in 90 countries. For 55 (31.4%) of the target 53.5%) caused medium, variable or heavy levels of weed species, only one biocontrol agent was intro- damage on the target weeds, and almost a quarter of duced. The largest number of agent species (44) was releases (225 or 23.9%) caused heavy impact. Across introduced for the biological control of Lantana all countries and regions, 65.7% of the weeds targeted camara (Verbenaceae). Three insect orders (Coleop- for biological control experienced some level of tera, Lepidoptera and Diptera) comprised about 80% control. These data indicate the value of this practice, of all biocontrol agent species released and releases on its own, or as a supplement to other methods, in the made. Of the 468 biocontrol agent species introduced, management of invasive plants. 332 (70.9%) established in at least one instance. Of the Keywords Weed biological control Establishment rates Impact Success rates Handling Editors: Cliff Moran and S. Raghu M. Schwarzla ¨nder (&) University of Idaho, Moscow, Idaho, USA e-mail: firstname.lastname@example.org Introduction H. L. Hinz Naturalized species are non-native species that form CABI, Dele ´mont, Switzerland self-sustaining populations following their introduc- R. L. Winston tion into an area outside their native distribution range MIA Consulting, Shelley, Idaho, USA (Richardson et al. 2000). More than 13,000 plant species, a little less than 4% of the world’s known M. D. Day vascular ﬂora, have become naturalized in at least one Queensland Department of Agriculture and Fisheries, region (Rejma ´nek 2015; van Kleunen et al. 2015). Mackay, Australia 123 320 M. Schwarzla ¨nder et al. Only a small proportion of naturalized plant species, Clewley et al. 2012; Culliney 2005; de Lange and van estimated at 1%, become detrimental in their intro- Wilgen 2010; Goeden 1988; Room et al. 1981; duced ranges (Williamson 1996; Williams and Fitter Suckling 2013; van Driesche et al. 2010). 1996). The invasive plants which do (namely, weeds) The ﬁrst global record of CBC releases for weeds can cause signiﬁcant economic damage to agriculture, was produced in the early 1980s (Julien 1982). The forestry and infrastructure (Beck et al. 2008; Pimentel publication titled ‘Biological control of weeds: a et al. 2005;Pysek et al. 2012) or threaten native world catalogue of agents and their target weeds’ biodiversity and ecosystem services (Pejchar and (henceforth ‘the catalog’) included data on the Mooney 2009;Pys ˇek et al. 2012; Vila et al. 2011), biological control agent species introduced for each all of which can ultimately impair human livelihoods targeted weed, the dates and countries of introduction (Shackleton et al. 2007). Chemical, mechanical and and measures of control efﬁcacy. The catalog was physical control methods have been the mainstay for subsequently updated and expanded approximately the management of weeds, especially in agricultural every ﬁve years until 1998 (Julien 1987, 1992; Julien settings (Kelton and Price 2009). However, conven- and Grifﬁths 1998). Because the catalog data were tional control methods are not economically viable for provided by weed biocontrol researchers themselves, a prolonged time or for the management of weeds in it is considered more accurate and complete than other remote areas or on vast tracts of publically owned compilations and has become the trusted source of lands with low agricultural value (Culliney 2005; information and the principal citation for release Sheley et al. 2011). Continuing globalization and records worldwide (McFadyen 1998). Every newly- intensiﬁed international trade will result in increased published edition of the catalog has also been used to naturalization of plant species outside their native evaluate trends of control successes or failures range (van Kleunen et al. 2015) and thus exacerbate (Crawley 1989; Cullen 1995; Heimpel and Mills the problem and the need for alternative management 2017; Julien 1989; Julien et al. 1984). Assessments of solutions to control weeds. the extent of control achieved, based on the catalog, Classical biological control (CBC) is an alternative are, however, limited due to the lack of a clear method for the management of non-native weeds deﬁnition of success and the fact that data are whereby host-speciﬁc, co-evolved natural enemies subjective and variable, depending on the sources (biological control agents) from the weed’s native (McFadyen 1998). range are reunited with the invasive plant in the In 2014, following a 16-year hiatus, a new (ﬁfth) introduced range. The aim of CBC is for introduced edition of the catalog was published (Winston et al. biological control agents to establish in their new 2014). Following the convention in previous versions, environment and increase in abundance to levels that the ﬁfth edition comprises three major tables: (1) inﬂict sufﬁcient damage to target weeds to reduce their intentional CBC introductions for weeds, (2) the use of competitiveness, reproductive output and population natural enemies, native to the area of introduction, to growth. Particularly in ecologically sensitive environ- control weeds, and (3) biocontrol agents that now ments, CBC can be a sustainable, self-perpetuating, occur in countries or regions in which they were not and effective control method for non-native weeds deliberately introduced. An additional table from (McFadyen 1998). The ﬁrst documented case of CBC previous editions of the catalog, based on exotic of a weed species dates back 182 years, when the vertebrates introduced to control weeds, was not cochineal insect Dactylopius ceylonicus (Green), included but has been replaced by a new table sum- originally and mistakenly brought from Brazil to marizing the use of bioherbicides (Winston et al. 2014, India in 1795 for dye production, was intentionally Table 4). The ﬁfth edition of the catalog has greatly moved from northern to southern India in 1836 and expanded the dataset: the number of targeted weed from India to Sri Lanka in 1865 to control Opuntia species has increased by 41% from 133 in the fourth monacantha (Willd.) Haw. (Cactaceae) (Goeden edition to 187 in the ﬁfth, and the number of biocontrol 1988). Since 1902, when Lantana camara L. sens. agent species deliberately released has increased by lat. (Verbenaceae) was targeted for CBC in Hawaii, 34% from 357 to 479. Due to the inclusion of more the discipline has yielded some impressive outcomes detailed data, the reference section increased from in a variety of environments (Bangsund et al. 1999; 123 Biological control of weeds: an analysis… 321 1084 records in the fourth edition to 2080 references The catalog is structured by release rather than listed in the ﬁfth edition. agent species. This is because numerous biocontrol In this paper, we provide a descriptive and numer- agent species were released in different countries/ ical analysis of CBC data derived exclusively from the regions, at various times and against different target ﬁfth edition of the catalog (Winston et al. 2014). In weeds. Separate releases of the same biocontrol agent conformity with the accounts derived from previous species, in different regions or countries, frequently editions (Crawley 1989; Julien et al. 1984; Julien resulted in different establishment success and were 1989), we too record the number of agent species also often associated with various degrees of damage released and releases made, their establishment rates, (impact) on their target host. Consequently, we present and their success rates over time, by agent taxon and establishment and impact data for agent species and by country or region of release. releases separately. Establishment and levels of target host damage Materials and methods (impacts) by the agents Source data Data on the establishment, or otherwise, of a release were taken from Table 1 in Winston et al. (2014). Although it may sometimes take many years before a We used the information from the ﬁfth edition of ‘‘Biological control of weeds: a world catalogue of biocontrol agent establishes, and decades before agent agents and their target weeds’’ (Winston et al. 2014)as population densities reach sufﬁcient levels to result in the data source for this account. We identiﬁed all cases weed control, i.e., a reduction in the density and/or where a weed biocontrol agent was intentionally distribution of the target plants (McFadyen 1998), we released through to the end of 2012. Releases were strictly followed the ‘impact’ categories used in treated as separate cases when any one of the Table 1 in Winston et al. (2014) for this analysis. following conditions was met: (1) a release of the Each biocontrol release made until the end of 2012 same agent occurred in different countries, (2) a that resulted in establishment was assigned one of release of the same agent was made in the same eight impact categories: ‘none’, ‘slight’, ‘medium’, country but from a different source location, (3) a ‘heavy’, ‘variable’, ‘too early post-release’, ‘un- release of the same agent was made in the same known’, or ‘compromised’. Releases made between country from the same source location, but for a 2007 and 2012 were typically assigned as ‘too early different target weed, or (4) a release of the same agent post-release’ and are not included in the analysis of was made in the same country, but more than impacts. We were primarily interested in releases that ﬁve years apart (Winston et al. 2014). Therefore, the caused the greatest amount of damage to the target number of identiﬁed biocontrol agent releases is far weeds, thus we only report cases in the three highest greater (n = 1555) than the number of biocontrol impact categories, namely ‘variable’, ‘medium’, and agent species that were released (n = 468). ‘heavy’. Impact categorizations were initially based Previous editions of the catalog have been consid- on subjective assessments by the data contributors. ered inconsistent and subjective because of their These were subsequently reviewed by the catalog reliance on information provided by individual bio- editors and amended where necessary for consistency. Final categorizations were supported by a brief control practitioners working on different biocontrol systems, and variable because data sources ranged description of the impact status for each release. from refereed publications to unpublished observa- In general, impact categories were deﬁned using tions (Heimpel and Mills 2017; McFadyen 1998). classiﬁcations similar to those used in previous Thus, for the ﬁfth edition of the catalog, the editors assessments of weed biocontrol program success, addressed these issues by deconstructing all previous which are based on the need for additional/other data and repopulating several new categorical ﬁelds control methods to supplement the degree of biocon- with many more data sources. As a consequence, data trol achieved (Hoffmann 1995; McFadyen 1998). If a in the ﬁfth edition of the catalog have been standard- biocontrol agent release resulted in heavy impact in ized (Winston et al. 2014). some countries/regions or at some sites and low or 123 322 M. Schwarzla ¨nder et al. medium impact in other countries/regions or at other regions, we deﬁned 11 main geographic divisions. We sites, we deﬁned this as ‘variable impact’. We deﬁned identiﬁed the ﬁve countries, continents or regions ‘medium impact’ as a biocontrol release that resulted historically and currently most active in weed biolog- in a reduced frequency or need for other control ical control: Australia, Hawaii, New Zealand (NZ), methods. When the need for other control methods North America (NA, including Canada, the USA, was stated as greatly reduced or no longer necessary, Mexico and Central America north of the Isthmus of the release was deﬁned as having ‘heavy impact’. To Panama) and South Africa. The remaining six geo- address impacts at the level of individual biocontrol graphic divisions included Asia, the remainder of agent species, multiple releases were combined Africa (including Ascension Island, Madagascar, (where applicable) and summarized. A biocontrol Mauritius and St. Helena), Oceania (including agent species was considered to have had variable, Melanesia, Micronesia and Polynesia), the Caribbean medium or heavy impact if this was true for at least Islands, South America and Eurasia (including the one of its releases in any given country or region. former Soviet Union in its post-1980 boundaries, e.g., In addition to agent impact, the catalog includes: (1) including Kazakhstan). agent-species abundance in seven categories, ‘rare’, ‘limited’, ‘moderate’, ‘high’, ‘variable’, ‘too early Biocontrol release history post-release’, and ‘unknown’, and (2) the extent of Biological control releases were tabulated in ten-year impact (to place agent impacts in a geographical context) in four categories, ‘localized’, ‘regional’, intervals with two exceptions: (1) all releases made ‘widespread throughout range’, and ‘unknown’ (Win- until 1900, regardless of when they occurred during ston et al. 2014). Categorizations were subjective the nineteenth century, were combined as one interval, decisions ﬁrst made by the data providers and and (2) the most recent time interval only included subsequently edited for consistency by the catalog three years (2010–2012). editors. Estimates of weed biocontrol program successes Results The majority of studies assessing the outcomes of Introductions and releases of weed biocontrol CBC of weeds use a terminology that differentiates agents between ‘negligible’, ‘substantial’ and ‘complete’ control of the target host (Hoffmann 1995; McFadyen Since the inception of CBC of weeds until 2012, a total 1998; Klein 2011). Because these are subjective of 468 agent species were intentionally released criteria that can be inﬂuenced by a broad range of worldwide in 1555 releases for the control of 175 factors (Heimpel and Mills 2017), the biological weed species in 48 plant families (Tables 1, 2). control outcomes for individual target weed species Lantana camara was the most highly targeted weed, were assessed as follows: a target weed was consid- with 44 biocontrol agents released against it. In ered ‘controlled’ if any release against that target host contrast, for 55 target weed species (31.4%), only a in a particular country/region led to variable, medium single biocontrol agent was introduced. Of the 468 or heavy impact. This approach obviously inﬂated the agent species intentionally released, 76 (16.2%) spread naturally or accidentally to other countries number of weeds targeted because the same weed species may be controlled in one but not in another (Table 3 in Winston et al. 2014). The ﬁve countries/ country or region. The numbers related to degrees of regions most active in biocontrol research and releases control were summarized for each geographical include, in decreasing order, Australia, NA, South region. Africa, Hawaii and NZ. These countries/regions accounted for 77.6% of all released agent species, or Countries and geographic regions 65.1% of all releases. For these countries/regions, there was a peak of agents released in the 1990s, To relate agent species introductions, establishment followed by a continuous decline (Fig. 1a). For all rates, impacts and control estimates to countries/ other countries/regions, agent numbers peaked 123 Biological control of weeds: an analysis… 323 Table 1 Number of agent species, releases, their establishment and impact among taxonomic groups of invertebrates and fungal pathogens released for classical biological control of weeds Groups No. agent No. Establishment Impact by agent Impact by release (no. species releases species (no. and % of and % of releases, d e released (%) species, n = 313 ) n = 940 ) (%) (No. and % of (No. and % of At best Medium, Heavy Medium, a b species , releases , heavy variable, variable, n = 468 total n = 1555 total or heavy or heavy species) releases) Insects (Insecta) Beetles 193 (41.3) 696 (44.8) 136 (70.5) 463 (66.5) 45 (35.4) 78 (61.4) 125 (27.7) 266 (59.0) (Coleoptera) Caterpillars 125 (26.7) 371 (23.9) 82 (65.6) 192 (51.8) 14 (17.5) 36 (45.0) 30 (16.1) 81 (43.5) (Lepidoptera) Flies (Diptera) 56 (12.0) 172 (11.1) 39 (69.6) 106 (61.6) 5 (13.2) 17 (44.7) 8 (7.8) 31 (30.1) Bugs and scales 35 (7.5) 185 (11.9) 28 (80.0) 129 (69.7) 11 (42.3) 17 (65.4) 49 (40.8) 87 (72.5) (Hemiptera) Sawﬂies, galling 10 (2.1) 18 (1.2) 8 (80.0) 13 (72.2) 3 (42.9) 4 (57.1) 5 (45.5) 6 (54.5) and seed- feeding wasps (Hymenoptera) Thrips 4 (0.9) 15 (0.97) 3 (75.0) 11 (73.3) 1 (33.3) 1 (33.3) 1 (9.1) 4 (36.4) (Thysanoptera) Grasshoppers 2 (0.4) 13 (0.84) 1 (50.0) 4 (30.8) 0 (0.0) 0 (0.0) 0 (0) 0 (0) (Orthoptera) True bugs 1 (0.2) 1 (0.06) 0 (0) 0 (0) 0 (0.0) 0 (0.0) 0 (0) 0 (0) (Heteroptera) Mites (Acarina) 10 (2.1) 28 (1.8) 9 (90.0) 22 (78.6) 0 (0.0) 4 (66.7) 0 (0) 6 (33.3) Nematodes 2 (0.4) 5 (0.32) 1 (50.0) 2 (40.0) 0 (0.0) 0 (0.0) 0 (0) 0 (0) (Nematoda) Fungal pathogens 30 (6.4) 51 (3.3) 25 (83.3) 40 (78.4) 5 (20.8) 15 (62.5) 7 (18.9) 22 (59.5) Total 468 (100) 1555 (100) 332 (70.9) 982 (63.2) 84 (26.8) 172 (55.0) 225 (23.9) 503 (53.5) Data summarized from Winston et al. (2014) Percentages calculated as the total number of biological control agent species (in a particular taxonomic group) that successfully established, divided by the total number of agent species released in that group Percentages calculated as the total number of releases (in a particular taxonomic group) that successfully established, divided by the total number of releases made in that group For deﬁnitions of variable, medium and heavy impact, see ‘‘Materials and methods’’ section Only species with at least one instance of conﬁrmed establishment and whose impact is not categorized as ‘too early post-release’ (n = 19) were considered (see text for details) Only releases conﬁrmed as established and whose impact is not categorized as ‘too early post-release’ (n = 42) were considered (see text for details) between the 1970s and 1990s, albeit at a much smaller Establishment of agent species scale, and were dominated by Africa in the 1970s and Asia in the 1990s (Fig. 1b), and subsequently declined Of 468 weed biocontrol agent species intentionally (Fig. 1b). Three insect orders (Coleoptera, Lepi- released, 332 (70.9%) established successfully. Of the total of 1555 intentional releases, 982 (63.2%) estab- doptera and Diptera) comprised 79.9% of all biocon- trol agent species released and 79.70% of all releases lished (Table 1). For biological control releases made prior to 1900, only 37.5% established, but after that made (Table 1). 123 324 M. Schwarzla ¨nder et al. Table 2 Number of agent species released, weeds targeted and controlled among taxonomic groups of invertebrates and fungal pathogens released for classical biological control of weeds Regions No. agent No. target No. agents % Agents No. target Percent target species weeds introduced established weeds weeds introduced per weed controlled controlled (%) Australia 202 56 3.6 67.8 39 69.6 North America 137 59 2.3 79.6 36 61.0 South Africa 103 51 2.0 69.9 38 74.5 Hawaii 87 22 4.0 67.8 13 59.1 Oceania 58 19 3.1 55.2 15 78.9 New Zealand 53 23 2.3 69.8 8 34.8 Asia 42 18 2.3 71.4 12 66.7 Africa 38 15 2.5 78.9 11 73.3 Caribbean 16 13 1.2 25.0 6 46.2 South America 14 10 1.4 64.3 3 30.0 Eurasia 10 5 2.0 40.0 0 0.0 a b c e 468 175 2.6 70.9 115 65.7 Data summarized from Winston et al. (2014) The sum of all introduced biocontrol agents across all regions (column total) equals n = 760 but includes duplicates (same species introduced in different areas) The total value is the number of all unique biocontrol agent species (n = 468) divided by the number of targeted weeds (n = 175) across all regions Percentages calculated as the total number of biological control agent species that established (n = 332), divided by the total number of agent species released (n = 468) A target weed was considered controlled in any given country or region if any release against this target in the same country or region resulted in variable, medium or heavy impact The sum of controlled target weed species across all regions (column total) equals n = 181 but includes duplicates (same target weeds successfully controlled in different countries/regions) establishment rates for releases were higher, ranging (53.5%) resulted in heavy, medium or variable from 53.7 to 76.9% (Fig. 2a). Release establishment impacts on the target weeds. Only 7.0% resulted in rates were consistent between countries/regions, with no impact at all. Of the 225 releases resulting in heavy the exception of the Caribbean and Eurasia, which had impact, 82.7% were associated with high agent notably lower release establishment rates of 35.1 and abundance. In 63.1% of heavy impact releases, the 37.5%, respectively (Fig. 2b). Biocontrol agent spe- impact was considered widespread throughout the cies establishment rates for the Caribbean and Eurasia range of the target weed. The proportion of releases were also lower at 25.0 and 40.0%, respectively with heavy impact was highest for the Caribbean, (Table 2). Of the various biocontrol agent taxa followed by Africa, Oceania, Asia and South Africa released, mites, fungal pathogens, Hymenoptera and (Fig. 3a). The numbers of releases with heavy impact Hemiptera (in that sequence) had the highest estab- were positively correlated with the numbers of estab- lishment rates at both the agent species and release lished releases among countries and regions (linear levels (Table 1). regression, r = 0.746, n =11, P = 0.008, Fig. 3b). Africa had the highest proportion of releases with Estimates of agent impacts and weed control heavy impact as a function of established releases achieved (Fig. 3b). In contrast, North America had the lowest proportion of releases with heavy impact (Fig. 3b). Of the 982 releases that established, 42 were consid- Of the 332 intentionally released agents that did ered to be too early post-release to accurately catego- establish, 19 were considered to be too early post- rize their impact. Of the 940 remaining releases, 503 release to categorize their impact. Of the 313 123 Biological control of weeds: an analysis… 325 Australia North America South Africa 90 Hawaii New Zealand -1900 1900s 1910s 1920s 1930s 1940s 1950s 1960s 1970s 1980s 1990s 2000s 2010s Oceania Asia Africa Carribean 12 South America Eurasia -1900 1900s 1910s 1920s 1930s 1940s 1950s 1960s 1970s 1980s 1990s 2000s 2010s Fig. 1 Number of new weed biological control agent species regions. The ﬁrst bar in each graph represents releases made introduced per decade: a for the ﬁve most active countries and between 1850 and 1900 and the last bar in each graph represents regions, and b for the less active remaining six countries/ releases made between 2010 and 2012 remaining species, 172 caused heavy, medium or considerably lower than the average for NZ, South variable impact in at least one release, i.e., 55.0% America and the Caribbean, and none of the ﬁve (Table 1). Hemiptera, Coleoptera and fungal patho- weeds targeted for CBC in Eurasia has been controlled gens were the biocontrol agent taxa with the highest (Table 2). proportions of agent species that caused heavy impact or a combination of medium, variable and heavy impact (Table 1). Discussion Biological control agents have been intentionally released against 175 weed species, of which 115 weed Measures of weed biocontrol activity over time species (65.7%) were controlled by at least one biocontrol agent species causing at least variable or During the 16 year period between the publication of medium impact (Table 2). Ninety-three or 53.1% of the ﬁrst and fourth editions of ‘Biological control of the target weeds were within three families, Aster- weeds: a world catalogue of agents and their target aceae, Cactaceae and Fabaceae (Table 3). The remain- weeds’ (Julien 1982; Julien and Grifﬁths 1998), the ing 82 weed species (46.9%) were distributed across number of weed species targeted for CBC increased by 45 different families. The ﬁve countries/regions with 51 (62.2%). In the 16 year period between the higher-than-average control rates were (ranked from publication of the fourth and ﬁfth editions, the number highest to lower) Oceania, South Africa, Africa, increased by 54 weed species (40.6%) (Winston et al. Australia and Asia. In contrast, the proportions of 2014). The number of new releases increased by 625 target weed species with some control were (125.2%) between the ﬁrst and fourth editions (Julien -1 No. new species released x decade 326 M. Schwarzla ¨nder et al. 100 a 60 b Africa Oceania North America 30 S. Africa Australia Asia Caribbean Hawaii New Zealand 0 50 100 150 200 250 No. releases established Fig. 3 Proportion of biological weed control releases with Fig. 2 Proportion of biological weed control releases estab- heavy impact a by region or country (? SE), and b as a function lished a by decade (± SE), with the overall mean (64.2 ± 3.2% of the number of releases established in a country or region, with SE) indicated by a line, and b by country or region (? SE) the line of best ﬁt indicated (linear regression, r = 0.746, n = 11, P = 0.008) 1982; Julien and Grifﬁths 1998), but only by 431 new releases (38.3%) between 1998 and 2014, i.e., between Rhinocyllus conicus Fro ¨ lich and Larinus carlinae the fourth and ﬁfth editions (Winston et al. 2014). The Olivier (both Curculionidae) on native Cirsium thistle lower rate of new releases can be explained by the species (Asteraceae) (Havens et al. 2012; Louda et al. decrease in new biocontrol agent species introduced 2005; Rose et al. 2005) as well as by Cactoblastis since the 1990s when 133 new species were released. cactorum (Berg) (Pyralidae) on some native Opuntia Data collection efforts continuing beyond the printing species (Cactaceae), including one threatened and of the ﬁfth edition indicate that globally, 42 new endangered species (Stiling et al. 2004). The ensuing agents were released between 2010 and 2017. Extrap- debate caused drastic tightening of the regulatory olating from this number suggests that there may only approval process, the consequences of which have be 50 or 51 new agent species released in the been discussed in detail, along with suggested steps to 2010–2019 decade, which would be 17.2% less than enhance progress in this ﬁeld of endeavor (Hinz et al. the 61 species released in the 2000s. 2014; Moran and Hoffmann 2015; Warner 2016). There are a number of factors contributing to the In Australia, the decrease in the rate of introduc- gradual decline in new biocontrol agent introductions. tions has been attributed mostly to funding cuts In the USA, the discipline has earned a negative (Palmer et al. 2014) and less to the debate about the reputation following reports of non-target attack by risks/beneﬁts associated with CBC of weeds. For -1900 1990s 1910s 1920s 1930s 1940s 1950s 1960s 1970s 1980s 1990s Australia 2000s North America South Africa Hawaii Oceania New Zealand Asia Africa Caribbean South America Eurasia Caribbean Africa Oceania Asia South Africa South America Australia North America Hawaii New Zealand Eurasia Percent releases established Percent releases established Percent releases with heavy impact No. releases with heavy impact Biological control of weeds: an analysis… 327 Table 3 Weeds targeted for classical biological control in respective plant families, successful control outcomes and rates of successful control Plant families No. of species with biological control Rate of successful control attempts Attempted Successful Amaranthaceae 1 1 1 Anacardiaceae 1 0 0 Apocynaceae 1 1 1 Araceae 1 1 1 Asparagaceae 1 1 1 Asteraceae 44 27 0.61 Azollaceae 1 1 1 Basellaceae 1 0 0 Bignoniaceae 2 1 0.50 Boraginaceae 5 4 0.80 Cactaceae 25 25 1 Caryophyllaceae 1 0 0 Chenopodiaceae 2 0 0 Commelinaceae 1 0 0 Convolvulaceae 5 1 0.20 Cucurbitaceae 1 1 1 Cyperaceae 1 0 0 Dioscoreaceae 1 0 0 Ericaceae 1 1 1 Euphorbiaceae 4 2 0.50 Fabaceae 23 16 0.70 Haloragaceae 1 1 1 Hydrocharitaceae 1 1 1 Hypericaceae 2 1 0.50 Lamiaceae 3 2 0.67 Loranthaceae 1 0 0 Lygodiaceae 1 0 0 Lythraceae 1 1 1 Malvaceae 2 2 1 Melastomataceae 3 2 0.67 Myricaceae 1 0 0 Myrtaceae 2 1 0.50 Orobanchaceae 3 0 0 Passiﬂoraceae 1 1 1 Plantaginaceae 2 2 1 Poaceae 1 0 0 Polygonaceae 5 4 0.80 Pontederiaceae 1 1 1 Proteaceae 2 1 0.50 Ranunculaceae 1 0 0 Rosaceae 6 4 0.67 Rubiaceae 1 0 0 Salviniaceae 1 1 1 123 328 M. Schwarzla ¨nder et al. Table 3 continued Plant families No. of species with biological control Rate of successful control attempts Attempted Successful Scrophulariaceae 1 0 0 Solanaceae 4 3 0.75 Tamaricaceae 1 1 1 Verbenaceae 2 1 0.50 Zygophyllaceae 2 2 1 Total 175 115 65.7 Families are listed alphabetically. Data summarized from Winston et al. (2014) Africa as a whole, Asia and Oceania in particular, and Coleoptera, supporting similar ﬁndings of an there appears to be a ﬂow-on effect, with reduced earlier analysis (Crawley 1989). capacity from Australia and elsewhere, and less funding in aid contributing to reduced CBC activities Efﬁcacy of weed biocontrol in these regions. In contrast, rates of biological control agent introductions are relatively stable for NZ and Because the catalog is structured by releases, we South Africa, where similar numbers of agent species assessed biocontrol agent efﬁcacy ﬁrst at the release were introduced in the 1990s and the 2000s/2010s. In level and from there deduced general impact for each these countries, CBC of weeds continues to thrive and of the 468 released biocontrol agent species. For the is enjoying broad public support (Martin et al. 2018; overall success, we calculated the proportion of Hayes et al. 2013; Hill and Coetzee 2017). biological control programs that have achieved some In assessments of earlier versions of the catalog, level of control, without further qualifying that control rates of agent establishment were calculated to be level. This is contrary to how most weed biological 71%, later revised to 63% for releases made until 1980 control program reviews assess success, which fre- (Julien 1989; Julien et al. 1984). The rates of agent quently utilize the deﬁnitions proposed by Hoffmann establishment were calculated at 65% (or 63% aver- (1995) and McFadyen (1998) and that distinguish aged out over decades) for releases made until 1985 between ‘negligible’, ‘partial’, ‘substantial’ and ‘com- (Julien 1989). Other analyses of previous versions of plete’ weed control. These categories have been the catalog have stated similar rates of establishment adopted by a number of regional assessments in for releases, ranging from 52 to 61% (Heimpel and Australia (Cullen et al. 2011; McFadyen 2000), New Mills 2017) to 63% (Crawley 1989). While some Zealand (Fowler et al. 2000; Hayes et al. 2013), South analyses record a decrease in recent establishment Africa (Hill and Coetzee 2017; Hoffmann 1995; Klein rates (Crawley 1989), others speculated that rates 2011; Moran et al. 2005), and Hawaii (Gardner et al. should increase because of improved release strategies 1995). The authors of those reviews are all weed and understanding of factors facilitating establishment biocontrol experts in their respective regions, and (McFadyen 1998 and references therein). Our account because they have access to additional information not was based on a much greater number of releases, and included in the catalog, they were able to assign also conﬁrmed agent establishment rates of 63.2%. program success ratings for each weed biocontrol The establishment rate based on the number of agent- system. Interestingly, the values reported here for the species involved was higher (70.9%). This is not percentages of target weeds controlled by countries surprising because agents released several times in and regions (Table 2) largely match those reported for different countries or regions have a higher probability Australia (Cullen et al. 2011), New Zealand (Hayes of establishing in at least some cases. Among the et al. 2013) and South Africa (Klein 2011). The overall major biocontrol agent taxa, we found that release- weed control rate of 65.7% derived from the present establishment failures were higher for species of analysis (see Table 2) is, however, much higher than Lepidoptera than for species in the Hemiptera, Diptera the 39.2% reported in Heimpel and Mills (2017). The 123 Biological control of weeds: an analysis… 329 and meticulousness that led to the publication of the ﬁrst four latter analysis was based on the fourth edition of the editions of the catalog and Brad Harmon for providing catalog, which may partially explain the discrepancy. information and comments improving an earlier draft of this The proportion of releases with ‘heavy’ impact was manuscript. The contribution of Hariet Hinz was supported by highest for the Caribbean, followed by Africa, Ocea- CABI with core ﬁnancial support from its member countries (see http://www.cabi.org/about-cabi/who-we-work-with/key- nia and Asia (Fig. 3a). Africa had the highest propor- donors/ for details). This is a publication of the Idaho Agricul- tion of releases with heavy impact as a function of tural Experimental Station. established releases (Fig. 3b). These results for the Caribbean, Africa and Asia can be explained by the Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http:// fact that many of the target weeds in these countries/ creativecommons.org/licenses/by/4.0/), which permits unre- regions were either cacti in the genus Opuntia,or stricted use, distribution, and reproduction in any medium, water weeds, both are categories of weeds which are provided you give appropriate credit to the original especially amenable to biological control (Crawley author(s) and the source, provide a link to the Creative Com- mons license, and indicate if changes were made. 1989; Hill and Coetzee 2017). 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Schwarzla¨nder is professor of entomology at the Univer- ping PW, van Klinken RD (2010) Classical biological sity of Idaho and investigates biocontrol in the context of control for the protection of natural ecosystems. Biol managing weeds of Eurasian origin in North America. He was Control 54:S2–S33 the chair of the symposium at the XXV International Congress van Kleunen M, Dawson W, Essl F, Pergl J, Winter M, Weber E, of Entomology (Orlando, USA) at which the papers in this Kreft H, Weigelt P, Kartesz J, Nishino M, Antonova LA, Special Issue were presented. Barcelona JF, Cabezas FJ, Cardenas D, Cardenas Toro J, Castano N, Chacon E, Chatelain C, Ebel AL, Figueiredo E, Fuentes N, Groom QJ, Henderson L, Singh I, Kupriyanov Hariet L. Hinz is the director of CABI in Switzerland as well A, Masciadri S, Meerman J, Morozova O, Moser D, as the leader of the Weed Biological Control Programme. 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