Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-11T01:35:54.123Z Has data issue: false hasContentIssue false

Successes We May Not Have Had: A Retrospective Analysis of Selected Weed Biological Control Agents in the United States

Published online by Cambridge University Press:  20 January 2017

Hariet L. Hinz*
Affiliation:
CABI Switzerland, Rue des Grillons 1, 2800 Delémont, Switzerland
Mark Schwarzländer
Affiliation:
Department of Plant Soil and Entomological Sciences, University of Idaho, Moscow ID, 83844-2339
André Gassmann
Affiliation:
CABI Switzerland, Rue des Grillons 1, 2800 Delémont, Switzerland
Robert S. Bourchier
Affiliation:
Agriculture and Agri-Food Canada, Lethbridge, Canada
*
Corresponding author's E-mail: h.hinz@cabi.org
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

In this paper, we describe five successful classical biological weed control agents released in the United States. For each of the five arthropod species, we compared data from prerelease studies that experimentally predicted the agent's host range with data collected postrelease. In general, experimental host range data accurately predicted or overestimated risks to nontarget plants. We compare the five cases with insects recently denied for introduction in the United States and conclude that none of the discussed agents would likely be approved if they were petitioned today. Three agents would be rejected because they potentially could attack economic plants, and two because of potential attack on threatened or endangered plants. All five biocontrol agents have contributed significantly to the successful management of major weeds with no or minimal environmental risk. We believe that the United States may miss opportunities for sustainable and environmentally benign management of weeds using biological control if the regulatory framework only considers the risks of agents as potential plant pests and treats any host-range data regarding economic or threatened and endangered species as a binary decision (i.e., mandates rejection if there is any chance of feeding or development). As a way forward we propose the following: (1) the addition of risk and benefit analyses at the habitat level with a clear ranking of decision-making criteria as part of the U.S. Department of Agriculture Animal and Plant Health Inspection Service Technical Advisory Group's evaluation process of biocontrol agents; (2) recognition of the primacy of realized host range data for potential agents that considers the insect's host selection behavior instead of emphasizing fundamental host range data during release evaluations, and (3) development of formalized postrelease monitoring of target and nontarget species as part of the release permit. These recommendations may initially be advanced through reassessment of current policies but may in the longer term require the implementation of dedicated biocontrol legislation.

Type
Research Article
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
Copyright © Weed Science Society of America

References

Literature Cited

Albach, DC, Meudt, HM, Oxelman, B (2005) Piecing together the “new” Plantaginaceae. Am J Bot 92:297315 Google Scholar
Andres, LA (1985) Interactions of Chrysolina quadrigemina and Hypericum species in California. Pages 235239 in Proceedings of the VI International Symposium on Biological Control of Weeds. Ottawa, Canada Agriculture Canada Google Scholar
Baker, JL, Webber, NAP, Johnson, KK (2004) Non-target impacts of Aphthona nigriscutis, a biological control agent for Euphorbia esula (leafy spurge), on a native plant Euphorbia robusta. Pages 247251 in Proceedings of the XI International Symposium on Biological Control of Weeds. Canberra, Australia CSIRO Entomology Google Scholar
Barratt, BIP, Moeed, A (2005) Environmental safety of biological control: policy and practice in New Zealand. Biol Control 35:247252 Google Scholar
Blossey, B, Casagrande, R, Tewksbury, L, Landis, DA, Wiedenmann, RN, Ellis, DR (2001) Nontarget feeding of leaf-beetles introduced to control purple loosestrife (Lythrum salicaria L.). Nat Areas J 21:368377 Google Scholar
Blossey, B, Schroeder, D, Hight, SD, Malecki, RA (1994) Host specificity and environmental impact of two leaf beetles (Galerucella calmariensis and G. pusilla) for biological control of purple loosestrife (Lythrum salicaria). Weed Sci 42:134140 Google Scholar
Boldt, PE, Rosenthal, SS, Srinivasan, R (1998) Distribution of field bindweed and hedge bindweed in the USA. J Prod Agric 11:377381 Google Scholar
Bredow, E, Pedrosa-Macedo, JH, Medal, JC, Cuda, JP (2007) Open field host specificity tests in Brazil for risk assessment of Metriona elatior (Coleoptera: Chrysomelidae), a potential biological control agent for Solanum viarum (Solanaceae) in Florida. Fla Entomol 90:559564 Google Scholar
Breiter, N, Seastedt, TR (2007) Postrelease evaluation of Mecinus janthinus host specificity, a biological control agent for invasive toadflax (Linaria spp.). Weed Sci. 55:164168 Google Scholar
Briese, DT (2004) Weed biological control: applying science to solve seemingly intractable problems. Aust J Ecol 43:304317 Google Scholar
Center, TD, Pratt, PD, Tipping, PW, Rayamajhi, MB, Van, TK, Wineriter, SA, Dray, FA Jr., (2007) Initial impacts and field validation of host range for Boreioglycaspis melaleucae Moore (Hemiptera: Psyllidae), a biological control agent of the invasive tree Melaleuca quinquenervia (Cav.) Blake (Myrtales: Myrtaceae: Leptospermoidaea). Environ Entomol 36:569576 Google Scholar
Clement, SL, Cristofaro, M (1995) Open-field tests in host-specificity determination of insects for biological control of weeds. Biocontrol Sci Technol 5:395406 Google Scholar
Cofrancesco, AF, Shearer, JF (2004) Technical Advisory Group for Biological Control Agents of Weeds. Pages 3841 in Coombs, EM, Clark, JK, Piper, GL, Cofrancesco, AF eds. Biological Control of Invasive Plants in the United States. Corvallis, OR Oregon State University Press Google Scholar
Corrigan, JE, Mackenzie, DL, Simser, L (1998) Field observations of non-target feeding by Galerucella calmariensis (Coleoptera: Chrysomelidae), an introduced biological control agent of purple loosestrife, Lythrum salicaria (Lythraceae). Pages 99106 in Proceedings of the Entomological Society of Ontario Vol. 129. Guelph, Ontario Entomological Society of Ontario Google Scholar
Cristofaro, M, De Biase, A, Smith, L (2013) Field release of a prospective biological control agent of weeds, Ceratapion basicorne, to evaluate potential risk to a nontarget crop. Biol Control 64:305314 Google Scholar
Cullen, JM, Delfosse, ES (1985) Echium plantigineum: catalyst for conflict and change in Australia. Pages 249292 in Proceedings of the VI International Symposium on Biological Control of Weeds. Ottawa, Canada Agriculture Canada Google Scholar
Currie, GA, Garthside, S (1932) The possibility of the entomological control of St. John's Wort in Australia. Melbourne, Australia Progress Rep. Council for Scientific and Industrial Research 29. 28 pGoogle Scholar
DeBach, P, Rosen, D (1991) Biological control by natural enemies. Cambridge, UK Cambridge University Press. 211 pGoogle Scholar
De Clerck-Floate, RA, Harris, P (2002) Linaria dalmatica (L.) Miller, Dalmatian toadflax (Scrophulariaceae). Pages 368374 in Mason, PG, Huber, JT eds. Biological Control Programmes in Canada, 1981–2000. Wallingford, UK CABI Publishing Google Scholar
Diaz, R, Manrique, V, Hibbard, K, Fox, AM, Roda, A, Gandolfo, D, McKay, F, Medal, J, Hight, S, Overholt, WA (2014) Successful biological control of tropical soda apple (Solanales: Solanaceae) in Florida: a review of key program components. Fla Entomol 1:179190 Google Scholar
Dudley, TL, Kazmer, DJ (2005) Field assessment of the risk posed by Diohabda elongata, a biocontrol agent for control of saltcedar (Tamarix spp.), to a nontarget plant Frankenia salina. Biol Control 35:265275 Google Scholar
Fernández-Mazuecos, M, Blanco-Pastor, J, Vargas, P (2013) A phylogeny of toadflaxes (Linaria Mill.) based on nuclear internal transcribed spacer sequences: systematic and evolutionary consequences. Int J Plant Sci 174:234249 Google Scholar
Fowler, SV, Gourlay, AH, Hill, RH, Withers, T (2004) Safety in New Zealand weed biocontrol: a retrospective analysis of host-specificity testing and the predictability of impacts on non-target plants. Pages 265270 in Proceedings of the XI International Symposium on Biological Control of Weeds. Canberra, Australia CSIRO Entomology Google Scholar
Frye, MJ, Lake, EC, Hough-Goldstein, J (2010) Field host-specificity of the mile-a-minute weevil, Rhinoncomimus latipes Korotyaev (Coleoptera: Curculionidae). Biol Control 55:234240 Google Scholar
Gandolfo, D, McKay, F, Medal, JC, Cuda, JP (2007) Open-field host specificity test of Gratiana boliviana (Coleoptera: Chrysomelidae), a biological control agent of tropical soda apple (Solanaceae) in the United States. Fla Entomol 90:223228 Google Scholar
Gaskin, JF, Bon, MC, Cock, MJW, Cristofaro, M, De Biase, A, De Clerck-Floate, R, Ellison, CA, Hinz, HL, Hufbauer, RA, Julien, MH, Sforza, R (2011) Applying molecular-based approaches to classical biological control of weeds. Biol Control 58:121 Google Scholar
Gassmann, A, Louda, SM (2001) Rhinocyllus conicus: initial evaluation and subsequent ecological impacts in North America. Pages 147183 in Wajnberg, E, Scott, JK, Quimby, PC eds. Evaluating Indirect Ecological Effects of Biological Control. Wallingford, UK CABI Publishing Google Scholar
Gassmann, A, Toševski, I, Speiwak, E, Heinlein, G, Rechner, H, Yaworski, K, Thalmann, M (2002) Biological Control of Toadflaxes, Linaria spp. Annual Report 2001. Delémont, Switzerland CABI Bioscience Switzerland Centre. 15 pGoogle Scholar
Groenteman, R, Fowler, SV, Sullivan, JJ (2011) St. John's wort beetles would not have been introduced to New Zealand now: a retrospective host range test of New Zealand's most successful weed biocontrol agents. Biol Control 57:5058 Google Scholar
Hill, R, Campbell, D, Hayes, L, Corin, S, Fowler, S (2013) Why the New Zealand regulatory system for introducing new biological control agents works. Pages 7583 in Proceedings of the XIII International Symposium on Biological Control of Weeds. Morgantown, West Virginia USDA Forest Service Forest Health Technology Enterprise Team Google Scholar
Holloway, JK (1948) Biological control of Klamath weed. Progress report. Econ Entomol 41:5657 Google Scholar
Huffaker, CB (1967) A comparison of the status of biological weed control of St. Johnswort in California and Australia. Mushi 39(suppl.):5173 Google Scholar
Huffaker, CB, Kennett, CE (1959) A ten-year study of vegetational changes associated with biological control of Klamath weed. J Range Manag 12:6982 Google Scholar
Jeanneret, P, Schroeder, D (1992) Biology and host specificity of Mecinus janthinus Germar (Col.: Curculionidae), a candidate for the biological control of yellow and Dalmatian toadflax, Linaria vulgaris (L.) Mill. and Linaria dalmatica (L.) Mill. (Scrophulariaceae) in North America. Biocontrol Sci Technol 2:2534 Google Scholar
Jensen, KIN, Harris, P, Sampson, MG (2002) Hypericum perforatum L., St John's wort (Clusiaceae). Pages 361368 in Mason, PG, Huber, JT eds. Biological Control Programmes in Canada, 1981–2000. Wallingford, UK CABI Publishing Google Scholar
Julien, MH, Griffiths, MW (1998) Biological Control of Weeds. A World Catalogue of Agents and their Target Weeds. 4th edn. Wallingford, UK CAB International. 223 pGoogle Scholar
Kok, LT, McAvoy, TJ, Malecki, RA, Hight, SD, Drea, JJ, Coulson, JR (1992) Host specificity tests of Galerucella calmariensis (L.) and G. pusilla (Duft.) (Coleoptera: Chrysomelidae), potential biological control agents of purple loosestrife, Lythrum salicaria L. (Lythraceae). Biol Control 2:282290 Google Scholar
Landis, DA, Sebolt, DC, Haas, MJ, Klepinger, M (2003) Establishment and impact of Galerucella calmariensis L. (Coleoptera: Chrysomelidae) on Lythrum salicaria L. and associated plant communities in Michigan. Biol Control 28:7891 Google Scholar
Lindgren, CJ, Corrigan, J, De Clerck-Floate, RA (2002) Lythrum salicaria L., purple loosestrife (Lythraceae). Pages 383390 in Mason, PG, Huber, JT eds. Biological Control Programmes in Canada, 1981–2000. Wallingford, UK CABI Publishing Google Scholar
Littlefield, JL (2004) Bindweeds. Pages 150151 in Coombs, EM, Clark, JK, Piper, GL, Cofrancesco, AF Jr, eds. Biological Control of Invasive Plants in the United States. Corvallis, Oregon Oregon State University Press Google Scholar
Louda, SM, Rand, TA, Arnett, AE, McClay, AS, Shea, K, McEachern, AK (2005a) Evaluation of ecological risk to populations of a threatened plant from an invasive biocontrol insect. Ecol Appl 15:234249 Google Scholar
Louda, SM, Rand, TA, Russell, FL, Arnett, AE (2005b) Assessment of ecological risks in weed biocontrol: input from retrospective ecological analyses. Biol. Control 35:253264 Google Scholar
McClay, AS, De Clerck-Floate, RA (2002a) Convolvulus arvensis L., field bindweed (Convolvulaceae). Pages 331337 in Mason, PG, Huber, JT eds. Biological Control Programmes in Canada, 1981–2000. Wallingford, UK CABI Publishing Google Scholar
McClay, AS, De Clerck-Floate, RA (2002b) Linaria vulgaris Miller, Yellow Toadflax (Scrophulariaceae). Pages 375382 in Mason, PG, Huber, JT eds. Biological Control Programmes in Canada, 1981–2000. Wallingford, UK CABI Publishing Google Scholar
McClay, AS, De Clerck-Floate, RA (2013) Convolvulus arvensis L., field bindweed (Convolvulaceae). Pages 307309 in Mason, PG, Gillespie, DR eds. Biological Control Programmes in Canada, 2001–2012. Wallingford, UK CABI Publishing Google Scholar
McFadyen, REC (1998) Biological control of weeds. Ann Review Entomol 43:369393 Google Scholar
McFadyen, RE, Vitelli, M, Setter, C (2002) Host specificity of the rubber vine moth, Euclasta whalleyi Popescu-Gorj and Constantinescu (Lepidoptera: Crambidae: Pyraustinae): field host-range compared to that predicted by laboratory tests. Aust J Entomol 41:321323 Google Scholar
Medal, J, Bustamante, N, Vitorino, M, Beal, L, Overholt, W, Diaz, R, Cuda, J (2010) Host specificity tests of Gratiana graminea (Coleoptera: Chrysomelidae), a potential biological control agent of tropical soda apple, Solanum viarum (Solanaceae). Fla Entomol 93:231242 Google Scholar
Medal, JC, Cuda, JP (2010) Establishment and initial impact of the leaf-beetle Gratiana boliviana (Chrysomelidae), first biocontrol agent released against tropical soda apple in Florida. Fla Entomol 93:493500 Google Scholar
Medal, J, Overholt, WA, Stansly, P, Roda, A, Osborne, L, Hibbard, K, Gaskalla, R, Burns, E, Chong, J, Sellers, B, Hight, SD, Cuda, JP, Vitorino, M, Bredow, E, Pedrosa-Macedo, JH, Wikler, C (2008) Establishment, spread and initial impacts of Gratiana boliviana (Chrysomelidae) on Solanum viarum in Florida. Pages 389393 in Proceedings of the XII International Symposium on Biological Control of Weeds. Wallingford, UK CABI International Google Scholar
Medal, JC, Pitelli, RA, Santana, A, Gandolfo, D, Gravena, R, Habeck, DH (1999) Host specificity of Metriona elatior, a potential biological control agent of tropical soda apple, Solanum viarum, in the USA. BioControl 44:421436 Google Scholar
Medal, JC, Sudbrink, D, Gandolfo, D, Ohashi, D, Cuda, JP (2002) Gratiana boliviana, a potential biocontrol agent of Solanum viarum: quarantine host-specificity testing in Florida and field surveys in South America. BioControl 47:445461 Google Scholar
Miller, ML, Aplet, GH (2005) Applying legal sunshine to the hidden regulation of biological control. Biol Control 35:358365 Google Scholar
Mullahey, JJ, Mislevy, P, Brown, WF, Kline, WN (1996) Tropical soda apple, an exotic weed threatening agriculture and natural systems. Dow Elanco. Down to Earth Vol. 51, No. 1. 8 pGoogle Scholar
Mullahey, JJ, Nee, M, Wunderlin, RP, Delaney, KR (1993) Tropical soda apple (Solanum viarum) : a new weed threat in subtropical regions. Weed Technol 7:783786 Google Scholar
Nowierski, RM (2004) Toadflax. Pages 379395 in Coombs, EM, Clark, JK, Piper, GL, Cofrancesco, AF Jr., eds. Biological Control of Invasive Plants in the United States. Corvallis, Oregon Oregon State University Press Google Scholar
Overholt, WA, Diaz, R, Hibbard, K, Roda, A, Amalin, D, Fox, A, Hight, SD, Medal, J, Stansly, P, Carlisle, B, Walter, J, Hogue, P, Gary, L, Wiggins, L, Kirby, C, Crawford, S (2009) Releases, distribution and abundance of Gratiana boliviana (Coleoptera: Chrysomelidae), a biological control agent for tropical soda apple (Solanum viarum, Solanaceae), in Florida. Fla Entomol 92:450457 Google Scholar
Overholt, WA, Diaz, R, Markle, L, Medal, JC (2010) The effect of Gratiana boliviana (Coleoptera: Chrysomelidae) herbivory on growth and population density of tropical soda apple (Solanum viarum) in Florida. Biocontrol Sci Technol 20:791807 Google Scholar
Paynter, Q, Fowler, SV, Gourlay, AH, Haines, ML, Harman, HM, Hona, SR, Peterson, PG, Smith, LA, Wilson-Davey, JRA, Winks, CJ, Withers, TM (2004) Safety in New Zealand weed biocontrol: a nationwide survey for impacts on non-target plants. NZ Plant Protect 57:102107 Google Scholar
Pemberton, RW (2000) Predictable risk to native plants in weed biological control. Oecologia 125:489494 Google Scholar
Piper, GL (2004) St. Johnswort. Pages 322334 in Coombs, EM, Clark, JK, Piper, GL, Cofrancesco, AF Jr., eds. Biological Control of Invasive Plants in the United States. Corvallis, Oregon Oregon State University Press Google Scholar
Piper, GL, Coombs, EM, Blossey, B, McEvoy, PB, Schooler, SS (2004) Purple loosestrife. Pages 281292 in Coombs, EM, Clark, JK, Piper, GL, Cofrancesco, AF Jr., eds. Biological Control of Invasive Plants in the United States. Corvallis, Oregon Oregon State University Press Google Scholar
Pratt, PD, Rayamajhi, MB, Center, TD, Tipping, PW, Wheeler, GS (2009) The ecological host range of an intentionally introduced herbivore: a comparison of predicted versus actual host use. Biol. Control 49:146153 Google Scholar
Rector, BG, De Biase, A, Cristofaro, M, Primerano, S, Belvedere, S, Antonini, G, Sobhian, R (2010) DNA Fingerprinting to improve data collection efficiency and yield in an open-field host-specificity test of a weed biological control candidate. Invasive Plant Sci Manag 3:429439 Google Scholar
Rosenthal, SS, Platts, BE (1990) Host specificity of Aceria (Eriophyes) malherbe, [Acari: Eriophyidae], a biological control agent for the weed, Convolvulus arvensis [Convolvulaceae]. Entomophaga 35:459463 Google Scholar
Salaudeen, T, Thomas, M, Harding, D (2012) II. Economics of tropical soda apple in Florida. Pages 1019 in Medal, J, Overholt, W, Charudattan, R, Mullahey, J, Gaskalla, R, Díaz, R, Cuda, J, eds. Tropical Soda Apple Management Plan. Gainesville, FL University of Florida-IFAS. Florida Department of Agriculture and Consumer Services-DPI. 87 pGoogle Scholar
Schaffner, U (2001) Host range testing of insects for biological weed control: how can it be better interpreted? BioScience 51:951959 Google Scholar
Schat, M, Sing, SE, Peterson, RKD, Menalled, FD, Weaver, DK (2011) Growth inhibition of Dalmatian toadflax, Linaria dalmatica (L.) Miller, in response to herbivory by the biological control agent Mecinus janthinus Germar. J Entomol Sci 46:232246 Google Scholar
Schooler, SS, Coombs, EM, McEvoy, P (2003) Nontarget effects on crepe myrtle by Galerucella pusilla and G. calmariensis (Chrysomelidae), used for biological control of purple loosestrife (Lythrum salicaria). Weed Sci 51:449455 Google Scholar
Sheppard, AW, Hill, R, DeClerck-Floate, RA, McClay, A, Olckers, T, Quimby, PC Jr, Zimmermann, HG (2003) A global review of risk-benefit-cost analysis for the introduction of classical biological control agents against weeds: a crisis in the making? Biocontrol News Inf 24:91N108N Google Scholar
Sheppard, AW, van Klinken, RD, Heard, TA (2005) Scientific advances in the analysis of direct risks of weed biological control agents to nontarget plants. Biol Control 35:215226 Google Scholar
Smith, JM (1958) Biological control of Klamath weed, Hypericum perforatum L., in British Columbia. Pages 561565 in Proceedings of the 10th International Congress of Entomology. Ottawa, Canada Mortimer Google Scholar
Smith, L (2007) Physiological host range of Ceratapion basicorne, a prospective biological control agent of Centaurea solsticialis (Asteraceae). Biological Control 41:120133 Google Scholar
Smith, L, de Lillo, E, Amrine, JW Jr., (2010) Effectiveness of eriophyid mites for biological control of weedy plants and challenges for future research. Exp Appl Acarol 51:115149 Google Scholar
Smith, L, Hayat, R, Cristofaro, M, Tronci, C, Tozlu, G, Lecce, F (2006) Assessment of risk of attack to safflower by Ceratapion basicorne (Coleoptera: Apionidae), a prospective biological control agent of Centaurea solstitialis (Asteraceae). Biol Control 36:337344 Google Scholar
Suckling, DM, Sforza, RFH (2014) What magnitude are observed non-target impacts from weed biocontrol? PLOS ONE 9:112 Google Scholar
Taylor, DBJ, Heard, TA, Paynter, Q, Spafford, H (2007) Nontarget effects of a weed biological control agent on a native plant in Northern Australia. Biol Control 42:2533 Google Scholar
Toševski, I, Caldara, R, Jović, J, Hernandez-Vera, G, Baviera, C, Gassmann, A, Emerson, BC (2011) Morphological, molecular and biological evidence reveal two cryptic species in Mecinus janthinus Germar (Coleoptera, Curculionidae), a successful biological control agent of Dalmatian toadflax, Linaria dalmatica (Lamiales, Plantaginaceae). Syst Entomol 36:741753 Google Scholar
Toševski, I, Mitrović, M, Krstić, O, Jović, J, Gassmann, A (2012) Biological Control of Dalmatian and Yellow Toadflaxes (Linaria dalmatica and L. vulgaris). Annual Report 2011. Delémont, Switzerland CABI Bioscience Switzerland Centre. 69 pGoogle Scholar
USDA. (2000) Reviewer's Manual for the Technical Advisory Group for Biological Control Agents of Weeds. Guidelines for Evaluating the Safety of Candidate Biological Control Agents. United States Department of Agriculture, Marketing and Regulatory Programs, Animal and Plant Health Inspection Service, Plant Protection and Quarantine, 1st Edition Google Scholar
USDA APHIS (2014) Technical Advisory Group for Biological Control Agents of Weeds TAG Petitions – APHIS Actions. http://www.aphis.usda.gov/plant_health/permits/tag/downloads/TAGPetitionAction.pdf. Accessed: November 13, 2014Google Scholar
Van Hezewijk, BH, Bourchier, RS, De Clerck-Floate, RA (2010) Regional-scale impact of the weed biocontrol agent Mecinus janthinus on Dalmatian toadflax (Linaria dalmatica). Biol Control 55:197202 Google Scholar
Van Klinken, RD, Edwards, OR (2002) Is host-specificity of weed biological control agents likely to evolve rapidly following establishment? Ecol Lett 5:590596 Google Scholar
Van Wilgen, BW, Moran, VB, Hoffmann, JH (2013) Some perspectives on the risks and benefits of biological control of invasive alien plants in the management of natural ecosystems. Environ Manag 52:531540 Google Scholar
Villegas, B (2009) Biological control of Dalmatian toadflax in California. Pages 5960 in Woods DM, ed. Biological Control Program 2008 Annual Summary. Sacramento, California California Department of Food and Agriculture Plant Health and Pest Prevention Services Google Scholar
Villegas, B, Gibbs, C, Donnelly, J (2011) A case of fortuitous biological control of Dalmatian toadflax in Susanville. Pages 6466 in Woods, DM, ed. Biological Control Program 2010 Annual Summary. Sacramento, California California Department of Food and Agriculture Plant Health and Pest Prevention Services Google Scholar
Wagner, V, Nelson, CR (2014) Herbicides can negatively affect seed performance in native plants. Restor Ecol 22:288291 Google Scholar
Waipara, N, Barton, J, Smith, LA, Harman, HM, Winks, C, Massey, B, Wilkie, JP, Gianotti, A, Cripps, MG (2009) Safety in New Zealand weed biocontrol: a nationwide pathogen survey for impacts on non-target plants. NZ Plant Protect 62:4149 Google Scholar
Wapshere, AJ (1989) A testing sequence for reducing rejection of potential biological control agents for weeds. Ann Appl Biol 114:515526 Google Scholar
Ward, SM, Fleischmann, CE, Turner, MF, Sing, SE (2009) Hybridization between invasive populations of Dalmatian toadflax (Linaria dalmatica) and yellow toadflax (Linaria vulgaris). Invasive Plant Sci Manag 2:369378 Google Scholar
Weed, AS, Schwarzländer, M (2014) Density dependence, precipitation and biological control agent herbivory influence landscape-scale dynamics of the invasive Eurasian plant Linaria dalmatica. J Appl Ecol 51:825834 Google Scholar
Willis, AJ, Berentson, PR, Ash, JE (2003) Impacts of a weed biocontrol agent on recovery from water stress in a target and non-target Hypericum species. J Appl Ecol 40:320333 Google Scholar
Winston, RL, Schwarzländer, M, Hinz, HL, Day, MD, Cock, MJW, Julien, MH (in press) Biological Control of Weeds: A World Catalogue of Agents and their Target Weeds. 5th edn. MorgantownWest Virginia USDA Forest Service, Forest Health Technology Enterprise Team. FHTET-2014-XX. 223 pGoogle Scholar
Wilson, LM, Sing, SE, Piper, GL, Hansen, RW, De Clerck-Floate, RA, MacKinnon, DK, Randall, C (2005) Biology and biological control of Dalmatian and yellow toadflax. Morgantown, West Virginia USDA Forest Service, Forest Health Technology Enterprise Team-05-13. 116 pGoogle Scholar
Zimmermann, HG, Moran, VC, Hoffmann, JH (2000) The renowned cactus moth, Cactoblastis cactorum: its natural history and threat to native Opuntia floras in Mexico and the United States of America. Divers Distrib 6:259269 Google Scholar
Zwölfer, H (1967) The Host Range, Distribution, and Life-History of Rhinocyllus conicus Fröl. (Col, Curculionidae). Progress Report. Delémont, Switerland CAB International Institute of Biological Control. 18 pGoogle Scholar