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This Article Was Originally Published in a Journal Published by Elsevier This article was originally published in a journal published by Elsevier, and the attached copy is provided by Elsevier for the author’s benefit and for the benefit of the author’s institution, for non-commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues that you know, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier’s permissions site at: http://www.elsevier.com/locate/permissionusematerial Biological Control 40 (2007) 370–385 www.elsevier.com/locate/ybcon Successful biological control of mist Xower (Ageratina riparia) in New Zealand: Agent establishment, impact and beneWts to the native Xora Jane Barton a,¤, Simon V. Fowler b, Alison F. Gianotti a, Chris J. Winks a, Maarten de Beurs c, Greg C. Arnold d, Guy Forrester b a Landcare Research, Private Bag 92170, Auckland, New Zealand b Landcare Research, P.O. Box 40, Lincoln, New Zealand c The University of Auckland, Private Bag 92019, Auckland, New Zealand d Landcare Research, Private Bag 11052, Palmerston North, New Zealand Received 18 August 2006; accepted 19 September 2006 Available online 26 September 2006 Abstract The white smut fungus (Entyloma ageratinae) and the gall Xy (Procecidochares alani) were released in New Zealand in 1998 and 2001 respectively to suppress mist Xower (Ageratina riparia). The fungus established and spread rapidly, crossing 80 km of sea to Great Barrier Island within 2 years. The mean number of P. alani galls increased exponentially to 1.96/stem at release sites, but dispersal was slow. The impact of the biocontrol agents was monitored once annually from 1998/99 to 2003/04, at up to 51 sites in the North Island. The mean percentage of live leaves infected with fungus rapidly reached nearly 60%. Maximum plant height declined signiWcantly. In heavy infesta- tions, mean percentage cover of mist Xower declined from 81 to 1.5%. Galls were only recorded towards the end of the impact study, and at low mean numbers. As mist Xower declined, the species richness and mean percentage cover of native plants increased. In contrast, the species richness and mean percentage cover of exotic plants (excluding mist Xower) did not change signiWcantly. Many plant species colo- nizing the plots were important native mid- or late-successional shrubs or trees. With few exceptions, the exotic plant species common in the plots were not weeds that appeared to threaten native forest habitats. There was only a weak “replacement weed eVect” from the potentially serious invader African club moss (Selaginella kraussiana). These data, together with reports of reduced threats to rare endemic plants from mist Xower, suggest this rapid, well-monitored weed biocontrol program was very successful. © 2007 Elsevier Inc. All rights reserved. Keywords: Mist Xower; Ageratina riparia; Entyloma ageratinae; Procecidochares alani; Biological control of weeds; Replacement weeds; Native regeneration 1. Introduction (Fowler et al., 2000a). This pattern of mixed, often rather poor, monitoring in weed biocontrol is not restricted to Releases of biological control agents against weeds in New Zealand: worldwide there are few quantitative studies New Zealand have always been monitored carefully to showing that populations of the target weed declined after assess whether agents established, and in some cases quan- biological control, and even fewer that went on to show a titative data on the damage that agents inXicted on the tar- beneWt in terms of replacement by more desirable plant spe- get weed have been gathered (Cameron et al., 1989; Fowler cies (Denslow and D’Antonio, 2005; Syrett et al., 2000). et al., 2000a; Memmott et al., 1997). However, good moni- Furthermore, the best studied and reported examples toring data on reductions in weed populations, and on what appear to involve weeds that were primarily aVecting eco- plant species replaced theAuthor's weed, are almost entirely lacking personalnomically productive rangeland copy such as St John’s wort Hypericum perforatum L. in the USA (HuVaker and Ken- V * Corresponding author. Present address: 467 Rotowaro Rd, RD 1, nett, 1959). More recently, exotic weeds that a ect indige- Huntly 3771, New Zealand. Fax: +64 7 828 6650. nous biodiversity have become increasingly targeted by E-mail address: [email protected] (J. Barton). biological and other control methods. For such weeds, the 1049-9644/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2006.09.010 J. Barton et al. / Biological Control 40 (2007) 370–385 371 lack of published data showing beneWcial or otherwise out- ern Australia. It is a perennial herb or subshrub, growing comes seems even more pronounced. For example, in New to »1 m tall. It prefers a warm, moist habitat, can grow in Zealand, despite increased resources being focused on sun or shade, produces numerous small white Xowers in exotic weeds aVecting indigenous biodiversity, we could the spring, and spreads by wind- and water-borne seeds. only Wnd a few examples where beneWts to the indigenous In New Zealand, mist Xower occurs as a weed of forest Xora were quantiWed after weed control of any sort: recov- margins, open places, poorly managed pasture, wetlands ery of indigenous plants after control of old man’s beard, and stream banks, mostly in the northern half of the Clematis vitalba L. (Ogle et al., 2000); mixed-short term North Island (Anonymous, 1999). Stock mostly avoid results after chemical control of Japanese honeysuckle grazing the plant, but it can be toxic to horses (O’Sullivan Lonicera japonica, climbing dock Rumex sagittatus Thunb., et al., 1985). It is also common beside walking tracks and and bone-seed Chrysanthemoides monilifera (L.) Norl. (Wil- along river systems in native forests, where it can form liams et al., 1998); and, unpublished beneWts to indigenous large, dense mats of semi-woody stems which smother plants in a sand dune ecosystem after chemical control of native plants and prevent their regeneration (Anonymous, marram grass Ammophila arenaria (L.) Link (M. Hilton 1999). In two speciWc examples, mist Xower was reported pers. comm.). This paucity of data on tangible beneWts to to be a threat to the survival of two endemic plants, Hebe indigenous plant communities after any form of weed con- bishopiana (Petrie) Hatch and Hebe acutiXora Cockayne trol appears to be a worldwide phenomenon, e.g., Luken (de Lange, 1996). H. bishopiana is endemic to the Waitak- (1996) states “unfortunately there are few studies where ere Ranges and is classiWed as nationally vulnerable, with long-term eVects of management practice, speciWcally plant the main threats being invasion of its habitat by mist removal, have been documented in terms of community Xower, and to a lesser extent the related weed A. adeno- response”. phora (Sprengel) R. King et H. Robinson and two exotic The recent introduction into New Zealand of two bio- pampas grasses, Cortaderia spp. (de Lange et al., 1999). control agents against the weed mist Xower, Ageratina ripa- The second threatened endemic plant species, H. acutiX- ria (Regel) R. King and H. Robinson (Asteraceae), ora, has been classiWed as nationally endangered or vul- provided an opportunity to monitor the impacts of these nerable over the last 15 years. Mist Xower had almost agents. Biocontrol agents were introduced to Hawai’i in the eliminated H. acutiXora from Kerikeri Falls, where it was 1970s where they quickly controlled mist Xower in range- Wrst collected, and had started invading the habitat of lands (Trujillo, 1985). It was hoped that similar rapid suc- H. acutiXora in nearby Puketi Forest (Fig. 1), its only cess would be achieved in New Zealand. In Hawai’i, four other known site (P. de Lange, Department of Conserva- biocontrol agents were released (Julien and GriYths, 1998), tion, New Zealand, personal communication). and three established; a white smut fungus, Entyloma ager- Given these impacts on indigenous Xora, it was consid- atinae Barreto and Evans (Ustilaginomycetes); a gall Xy, ered particularly important to monitor the success or oth- Procecidochares alani Steyskal (Tephritidae); and a plume erwise of the mist Xower biological control program in moth Oidaematophorus beneWcus Yano and Heppner New Zealand. In addition, the importance of having good (Pterophoridae). These agents reportedly greatly reduced assessment data from new weed biocontrol programs can- mist Xower populations, thus rehabilitating the rangelands not be overemphasized, particularly given the much more (Trujillo, 1985), and although quantitative monitoring data rigorous assessment of environmental risks/beneWts in are lacking, this project is regarded as highly successful modern applications to release biocontrol agents in New (Evans, 2002; Julien and GriYths, 1998; Morin et al., 1997; Zealand (Fowler et al., 2000b). The aims of this monitor- Rosskopf et al., 1999). ing program were to (1) assess agent establishment and Morin et al. (1997) compared climate data from sites in dispersal; (2) measure the levels of attack by the agents Hawai’i where mist Xower was eVectively biologically con- and changes to mist Xower infestations; and (3) monitor trolled, with data from areas in New Zealand where the changes in native and exotic vegetation if mist Xower was weed was causing problems, and concluded that the bio- suppressed. This paper presents the Wnal analyses of this control agents should be active in the latter. It was recom- monitoring program following on from the preliminary mended that the fungus and the gall Xy should be reports in Fröhlich et al. (2000) and Barton née Fröhlich introduced to New Zealand, and that if needed, the plume et al.
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