Exp Appl Acarol (2010) 51:115–149 DOI 10.1007/s10493-009-9299-2 Effectiveness of eriophyid mites for biological control of weedy plants and challenges for future research L. Smith Æ E. de Lillo Æ J. W. Amrine Jr. Received: 31 March 2009 / Accepted: 3 August 2009 / Published online: 16 September 2009 Ó Springer Science+Business Media B.V. 2009 Abstract Eriophyid mites have been considered to have a high potential for use as classical biological control agents of weeds. We reviewed known examples of the use of eriophyid mites to control weedy plants to learn how effective they have been. In the past 13 years, since Rosenthal’s 1996 review, 13 species have undergone some degree of pre- release evaluation (Aceria genistae, A. lantanae, Aceria sp. [boneseed leaf buckle mite (BLBM)], A. salsolae, A. sobhiani, A. solstitialis, A. tamaricis, A. thalgi, A. thessalonicae, Cecidophyes rouhollahi, Floracarus perrepae, Leipothrix dipsacivagus and L. knautiae), but only four (A. genistae, Aceria sp. [BLBM], C. rouhollahi and F. perrepae) have been authorized for introduction. Prior to this, three species (Aceria chondrillae, A. malherbae and Aculus hyperici) were introduced and have become established. Although these three species impact the fitness of their host plant, it is not clear how much they have contributed to reduction of the population of the target weed. In some cases, natural enemies, resistant plant genotypes, and adverse abiotic conditions have reduced the ability of eriophyid mites to control target weed populations. Some eriophyid mites that are highly coevolved with their host plant may be poor prospects for biological control because of host plant resis- tance or tolerance of the plant to the mite. Susceptibility of eriophyids to predators and pathogens may also prevent them from achieving population densities necessary to reduce host plant populations. Short generation time, high intrinsic rate of increase and high mobility by aerial dispersal imply that eriophyids should have rapid rates of evolution. This raises concerns that eriophyids may be more likely to lose efficacy over time due to coevolution with the target weed or that they may be more likely to adapt to nontarget host plants compared to insects, which have a longer generation time and slower population L. Smith (&) USDA-ARS Western Regional Research Center, 800 Buchanan Street, Albany, CA 94710, USA e-mail: [email protected] E. de Lillo Dipartimento di Biologia e Chimica Agroforestale e Ambientale, Facolta` di Agraria, Universita` Bari, Italy, via Amendola, 165/A, 70126 Bari, Italy J. W. Amrine Jr. Department of Biology, West Virginia University, 53 Campus Dr., Morgantown, WV 26506, USA 123 116 Exp Appl Acarol (2010) 51:115–149 growth rate. Critical areas for future research include life history, foraging and dispersal behavior, mechanisms controlling host plant specificity, and evolutionary stability of eri- ophyid mites. This knowledge is critical for designing and interpreting laboratory and field experiments to measure host plant specificity and potential impact on target and nontarget plants, which must be known before they can be approved for release. One of the more successful examples of an eriophyid mite controlling an invasive alien weed is Phyllo- coptes fructiphilus, whose impact is primarily due to transmission of a virus pathogenic to the target, Rosa multiflora. Neither the mite nor the virus originated from the target weed, which suggests that using ‘‘novel enemies’’ may sometimes be an effective strategy for using eriophyid mites. Keywords Biocontrol Á Invasive plant Á Weed Á Host plant specificity Á Efficacy Introduction Classical biological control involves the importation and release of host-specific natural enemies to help regulate pest populations (Goeden and Andres 1999; van Driesche et al. 2008). This strategy is generally applied against invasive alien species that lack effective natural enemies in the adventive region. In order to avoid direct damage to nontarget species, biological control agents must be highly host specific. About 80% of currently known species of eriophyoid mites have been recorded in association with a single species of host plant (Skoracka et al. (2009) in this issue). There are about 4,000 recognized species, 25% of which were named in the last 12 years, suggesting that many more remain to be discovered (de Lillo and Skoracka (2009) in this issue). Thus, there should be a large number of prospective agents available to discover. In order to be effective and to mini- mize indirect nontarget impacts, biological control agents must significantly reduce fitness of the target weed (McClay and Balciunas 2005; Smith 2006). Eriophyoid mites can substantially damage vegetative and reproductive plant parts, have high reproductive rates, and disperse widely by wind, which all favor their potential to be effective biological control agents (Rosen and Huffaker 1983; Lindquist et al. 1996; Briese and Cullen 2001). Thus, eriophyoid mites have long been thought to have a high potential as a source for biological control agents of weeds, and many review papers have promoted their prospects (Cromroy 1977, 1983; Andres 1983; Boczek 1995; Boczek and Petanovic´ 1996; Petanovic´ 1996; Rosenthal 1996; Briese and Cullen 2001; Cullen and Briese 2001; Gerson et al. 2003). On the other hand, relatively few species of eriophyoids are considered economic pests (Lindquist et al. 1996; Hong et al. 2001), which suggests that the impact of most species is limited by factors such as host plant resistance or tolerance, natural enemies, and adverse abiotic conditions, which are the same factors that limit efficacy of biological control agents (Smith 2004). At present, relatively few eriophyoid species actually have undergone evaluation, governmental approval and introduction to new regions, and few of these have significantly reduced populations of the target weed. In her 1996 review, Rosenthal discussed eight species of eriophyids with high potential. Briese and Cullen (2001) listed 29 species of eriophyid mites considered to have potential as biological control agents. However, today we find that only three of these species have been successfully intentionally introduced to other countries for classical biological control: Aceria malherbae Nuzzaci, Aceria chondrillae (Canestrini) and Aculus hyperici (Liro), all of which had been used before 123 Exp Appl Acarol (2010) 51:115–149 117 1996. Briese and Cullen (2001) reported that all three of these mites had measurable impact on the target plant, but that only A. chondrillae had been a major contributor to control. Since Briese and Cullen’s (2001) review, at least 13 other species have undergone pre-release evaluations, but only Aceria genistae (Nalepa), the boneseed leaf buckle mite (Aceria sp., which needs taxonomical evaluation), A. lantanae (Cook), Cecidophyes rou- hollahi Craemer and Floracarus perrepae Knihinicki and Boczek, have been approved for release. Are eriophyid mites proving to be less useful than previously thought, and if so, what can be done to improve our ability to use them? The purpose of this paper is to review the status of eriophyid mites as safe, effective biological control agents and to consider what areas of research are needed to improve our ability to evaluate and use these organisms for classical biological control of weeds. Here we present a more detailed treatment of some of the information and ideas in Smith et al. (2008). Status of introduced eriophyids In this section we discuss species that have been officially approved for release as classical biological control agents. Aceria chondrillae, A. malherbae and Aculus hyperici are the oldest cases of attempts to use eriophyid mites for biological control. More information on these projects can be found summarized in Rosenthal (1996), Briese and Cullen (2001) and Gerson et al. (2003). Aceria chondrillae is native to Europe and has been introduced to control Chondrilla juncea L. (rush skeletonweed, Asteraceae) in Australia, the USA and Argentina (Cullen et al. 1982; Piper and Andres 1995; Cordo 1996; Cullen and Briese 2001). The plant has at least four different genotypes that vary in resistance to the mite, so it was necessary to find strains of the mite suitable for the various ‘‘forms’’ of the plant (Sobhian and Andres 1978; Cullen and Moore 1983). A Greek strain induced galls on two of the three Australian plant forms, but not on accessions from North America. The Vieste, Italy strain of the mite induced galls on all three N. American plant accessions tested, but not on the Australian narrow-leaf form. In California, the introduced mite is widespread and densities can be high in Sacramento and Eldorado counties (B. Villegas pers. comm.), but its effectiveness may be limited by the predatory mite, Typhlodromus pyri Scheuten (Phytoseiidae) (Piper and Andres 1995). In Idaho, A. chondrillae is widespread and appears to be limited by the cold winter weather which causes high mortality and by lack of rosettes in the fall on north- facing slopes (Milan et al. 2006; T. Prather pers. comm.). The mite is widespread in Oregon and Washington, and in some areas it may reduce flowering and seed production by 50–90%, depending on plant size and environmental conditions (E. Coombs pers. comm.). It does best in dry areas and where deer do not graze the early growth of the host plant. In Washington State, the weed has been successfully controlled in some areas, and A. chondrillae is considered to be the most effective of the three biological control agents that were released (Piper 1985; Piper et al. 2004). In Montana, rush skeletonweed is under eradication; however, the mite has been observed in several isolated C. juncea infestations in northwestern portions of the state (J. Littlefield pers. comm.). The mite is established in the Okanagan and Kootanay valleys of British Columbia, Canada, but the weed popula- tions are persisting (R. De Clerck-Floate pers. comm.). In late September at Vernon, only about 10% of flower heads were distorted, a few plants were stunted, and it generally appears that the mite only establishes at sites where it has been released (P.