J. Appl. Entomol. 130(9-10), 473–479 (2006) doi: 10.1111/j.1439-0418.2006.01090.x  2006 The Authors Journal compilation  2006 Blackwell Verlag, Berlin

Winter mortality of Aceria chondrillae, a biological control agent released to control rush skeletonweed (Chondrilla juncea) in the western United States J. D. Milan, B. L. Harmon, T. S. Prather and M. Schwarzla¨nder Division of Entomology, Department of Plant Soil and Entomological Sciences, University of Idaho, Moscow, ID, USA Ms. received: April 18, 2006; accepted: July 14, 2006

Abstract: Classical biological control of weeds is based on the assumptions that: (1) plant species are in part invasive in their introduced range because of the absence of coevolved specialist herbivore arthropods and plant pathogens; and (2) that these specialist herbivores can regulate host-plant populations. Although the need for quantitative post-release monitoring studies testing these assumptions has been acknowledged repeatedly, the number of assessments is still remarkably small and usually restricted to systems with notable impact of an agent species. However, studying systems where biological control agents cause no observable target weed reductions may be important to identifying factors that limit the population size or impact of biological control agents. Three biological agents were released for the control of the herbaceous perennial rush skeletonweed, Chondrilla juncea in North America between 1975 and 1977. Although all three species are widely established, weed densities are increasing and there is little quantitative information on factors limiting biological control efficacy. We examined the winter biology and survivorship of the rush skeletonweed gall mite Aceria chondrillae at two rush skeletonweed field sites in south-western Idaho over 2 years. Gall mite winter mortality was high (>90%) in both years and for both sites. Gall mites were more abundant on plants that produced rosettes in fall and rush skeletonweed plants growing on southern aspect were 3.4 times more likely to produce rosettes than those growing on northern aspects. Our data suggest that A. chondrillae population densities are limited by its high winter mortality. The gall mites may require fall rosettes to successfully survive the winter, which are commonly absent on north-facing aspects, impairing the efficacy of A. chondrillae to control rush skeletonweed in the intermountain western United States.

Keywords: agent impact, fall rosette presence, slope aspect, winter biology

1 Introduction Biological control programmes have traditionally been focused on finding, screening, releasing and distributing organisms (Blossey 1995a; McClay 1995; Briese 1996; McEvoy and Coombs 1999; Louda 2000; Goolsby et al. 2004). Although a few notable impact studies have been conducted (McEvoy et al. 1991; Hight et al. 1995; Hunt-Joshi et al. 2004; Hunt-Joshi and Blossey 2005), post-release quantitative monitoring rarely occurs despite decades of acknowledging the need for such monitoring (Schroeder 1983). The lack of data on the effects of biological control agents on their target host plants limits scientific improvements of biological weed control (Blossey and Skinner 2000). Long-term evaluations are an essential component of monitoring programmes that will enable scientists to increase success rates, gain predictability and avoid trial-and-error approaches that are still prevalent in weed biological control programmes (Lawton 1990; McFadyen 1998; McEvoy and Coombs 1999).

Rush skeletonweed, Chondrillae juncea L., is a rhizomatous herbaceous perennial of the Asteraceae family native to the Mediterranean (Hitchcock and Cronquist 1973) that currently infests more than 2.5 million hectares of cropland, right-of-ways, rangeland and semiarid pastureland in the western United States (Sheley et al. 1999). A biological control programme for rush skeletonweed identified and approved four biological control agents for release in Australia in the 1970s and these agents were later approved in the United States (Caresche and Wapshere 1974; Andres 1982). Three of those agents, the gall midge, Cystiphora schmidti Ru¨bsamen (Dipt., Cecidomyiidae), the rust fungus, Puccinia chondrillina Bubak and Sydenham, and the gall mite, Aceria chondrillae (Canestrini) [¼ Eriophyes chondrillae Canestrini] (Acari, Eriophyidae) (Amrine and Stasny 1994) are now widely established in Australia and the United States and offer various degrees of control (Cullen 1974; Dimock 1982; Piper and Andres 1995; Julien and Griffiths 1998; Coombs

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et al. 2004). The fourth agent, the root-boring moth, Bradyrrhoa gilveolella Treitschke (Lep., Phycitidae) did not establish itself in Australia (Cullen 1980) and it has only recently been released in North America (H. Prody, Montana State University, unpublished data). One of the biological control agents, the rush skeletonweed mite, A. chondrillae, induces gall formation of the vegetative and floral buds, which greatly reduces seed production and stunts plants (Cullen et al. 1982). A. chondrillae was first introduced into Idaho in 1977 (Andres 1982) and is now widely established (Piper and Andres 1995). In the laboratory, A. chondrillae was found to be the most effective of the three established biological control agents, although the impact has not been quantified in the field (Piper 1985; Piper and Andres 1995). In addition, there is anecdotal information from studies in Australia and the US suggesting that mite populations crash during the winter, limiting their impact on rush skeletonweed populations (Caresche and Wapshere 1974; Cullen et al. 1982; Lee 1986). Potential factors affecting the winter survival of the gall mite have not been reported, although it is assumed that A. chondrillae crawl down the old stems to newly formed rosettes for overwintering and, thus would need these structures for survival (Caresche and Wapshere 1974). To examine the winter survival of A. chondrillae, we followed gall mite population numbers at field sites in south-western Idaho through the winter months to determine population decline and envrironmental factors that might be associated with the population decline. We had two specific hypotheses: (1) A. chondrillae suffers high winter mortality at field sites in south-western Idaho; (2) A. chondrillae winter survival is higher on rush skeletonweed plants that do form fall rosettes. A third hypothesis was tested following the first field season because of observations made during the first winter of study: (3) rush skeletonweed plants on southern aspects are more likely to produce fall rosettes than plants on northern aspects.

2 Materials and Methods 2.1 Study organisms Rush skeletonweed seeds germinate in fall or spring to form rosettes and rosettes grow from rootstocks in fall or early spring (Sheley et al. 1999). Plants generally overwinter as rosettes or as rootstocks and resume growth as soon as temperatures rise above freezing, bolting in late spring (Hull and Groves 1973; Wapshere et al. 1974, 1976; Groves and Cullen 1981; Prather 1993). Flowering, seed set and dispersal begin in early summer and continue until fall. Seeds mature within 9–15 days after flowers open (Sheley et al. 1999). Rush skeletonweed is an obligate apomict, resulting in populations that consist of many clones from a few genetically differing individuals (Wells 1971). Plants can also produce new shoots from severed root fragments, which can reach the surface even if buried up to 1.2 m deep (Sheley et al. 1999). Under moist conditions, new plants can grow from cuttings as small as 1.25 cm wide and 2.5 cm long (Sheley et al. 1999). Rush skeletonweed is mostly found on south- or west-facing slopes where well-drained sandy or gravelly soils predominate (Spollen 1986). Currently, in the

J. D. Milan et al. US, there are three recognized biotypes of rush skeletonweed: (1) Washington early-flowering, (2) Washington late-flowering and (3) Banks (Old 1981), although studies to determine the validity of these biotypes are on-going (M. Schwarzla¨nder, University of Idaho and J. Gaskin, Agriculture Research Service, Sidney, MT, unpublished data). The biology A. chondrillae was summarized by Caresche and Wapshere (1974). In summary, A. chondrillae produces leafy, hyperplastic galls from vegetative and flower buds of rush skeletonweed. In spring, A. chondrillae are lifted with bolting flower stems and females begin to pierce the terminal and young axillary buds with stylets of their rostrum, which contain cecidogenic chemicals (Caresche and Wapshere 1974). Females begin to reproduce after hyperplastic tissues start to form. A. chondrillae reproduce sexually, but without copulation: males produce spermatophores that the females then draw into their genital orifice (Caresche and Wapshere 1974). Females lay a small number of soft round eggs. The development of the mite is rapid with one generation completed in