(Diptera: Agromyzidae) and Fusarium Spp

REVIEW & INTERPRETATION

Constraints on Asparagus Production: The Association of Ophiomyia simplex (Diptera: Agromyzidae) and Fusarium spp.

William R. Morrison III,* Julianna K. Tuell, Mary K. Hausbeck, and Zso' a Szendrei

W.R. Morrison III, J.K. Tuell, and Z. Szendrei, Dep. of Entomology, ABSTRACT Michigan State Univ., 243 Natural Science, East Lansing, MI 48824- Production of asparagus (Asparagus ofﬁ cinalis 1311; M.K. Hausbeck, Dep. of Plant Pathology, Michigan State Univ., L.) is globally constrained by the “early decline” 107 Center for Integrated Plant Systems, East Lansing, MI 48824-1115. syndrome. The primary causal agents of early Received 14 Feb. 2011. *Corresponding author ([email protected]). decline include Fusarium proliferatum (Matsu- Abbreviations: FCRR, Fusarium crown and root rot; IPM, inte- shima) Nirenberg, F. oxysporum Wollenw. f. sp. grated pest management. asparagi S.I. Cohen, and F. subglutinans Wol- lenw. & Reinking. These pathogens together contribute to Fusarium crown and root rot !"#$#%&! (Asparagus o! cinalis L.) production has become (FCRR). Damage to asparagus stems, especially Aincreasingly constrained globally during the past several by the asparagus miner (Ophiomyia simplex decades because of problems with replanting asparagus ' elds and Loew [Diptera: Agromyzidae]), has been associ- the early onset of asparagus stand decline (Grogan and Kimble, ated with and shown to exacerbate FCRR. This 1959; Elmer et al., 1996). Grogan and Kimble (1959, p. 122) review synthesizes the current information on de' ned asparagus decline as “a slow decline in the productiv- this tripartite interaction, describes manage- ity of old asparagus plantings … to the point where the plant- ment strategies and their ef! cacy, and high- ings become unpro' table to maintain.” The authors furthermore lights needed research. Opportunities for future de' ned the replant problem as “the inability to establish produc- control of the asparagus miner and associated FCRR are presented. Research areas of interest tive plantings … where plantings have declined” (Grogan and include investigating the role of semiochemicals Kimble, 1959, p. 122). Early decline of asparagus can lead to a in the asparagus miner–Fusarium spp. interac- reduction in the lifespan of planted ' elds by 5 to 8 yr; farmers tion, identifying effective biological controls for are not able to recoup the investment associated with establishing the asparagus miner, and determining source asparagus ' elds (Elmer et al., 1996). populations of asparagus miner in new aspara- The fungi Fusarium subglutinans Wollenw. & Reinking, Fusar- gus plantings. ium proliferatum (Matsushima) Nirenberg (population D, Gibber- ella fujikuroi; Elmer, 1995), and Fusarium oxysporum Wollenw. f. sp. asparagi S.I. Cohen have been directly linked as partial causal agents in the premature decline (Keulder, 1999) and in the inability of new plantings to become established and be productive in locations where asparagus was previously grown (Grogan and Kimble, 1959; Elmer et al., 1996), even decades after asparagus

Published in Crop Sci. 51:1414–1423 (2011). doi: 10.2135/cropsci2011.01.0032 Published online 27 May 2011. © Crop Science Society of America | 5585 Guilford Rd., Madison, WI 53711 USA All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher.

1414 WWW.CROPS.ORG CROP SCIENCE, VOL. 51, JULY–AUGUST 2011 was last grown (Poll and Huiskamp, 1992). The asparagus Fusarium spp. are anamorphic (Gordon and Martyn, miner, Ophiomyia simplex Loew (Diptera: Agromyzidae), 1997) and nearly ubiquitous in both agricultural soils and acts as a putative vector for infection of asparagus plants native soils around the world (Hartung et al., 1990; Vuja- with Fusarium. The larvae cause damage to the plant (Tuell novic et al., 2006). Both pathogenic and nonpathogenic and Hausbeck, 2008), exacerbating the early decline of strains of Fusarium spp. can be found in soils, even those that asparagus ' elds (Gilbertson et al., 1985). have not been planted to asparagus (Hartung et al., 1990). The purpose of this review is to examine and synthe- Fusarium oxysporum may infect young feeder roots, gaining size the current information about this tripartite interac- entry at the junction where the feeder roots emerge (Gra- tion between asparagus, the Fusarium spp. associated with ham, 1955; Smith and Peterson, 1983) between epidermal Fusarium crown and root rot (FCRR), and the asparagus cells. Subsequently, the fungus moves into the cells, radiating miner. We examine potential methods to limit the aspara- intercellularly into the cortex of the root. Lesions that are gus miner and thereby reduce FCRR, and discuss future small, red, and elliptical develop on the feeder root tips and research areas, including the need for an integrated pest along the root (Shoemaker, 1965 cf. Elmer, 2001), and may management (IPM) approach. also be evident on the underground portion of the plant stem. Asparagus that is damaged or stressed from cultural practices METHODS or other means is more susceptible to FCRR (Nigh, 1990). This review is a synthesis of information regarding FCRR Di) erent species of Fusarium are found in varying and the asparagus miner. The Michigan State University regions in the world: for example, in the Netherlands, F. library collection and online databases, including Web of culmorum (W.G. Sm.) Sacc. is associated with FCRR, while Science, ScienceDirect, SpringerLink, Google Scholar, and F. proliferatum and F. oxysporum are absent (Blok and Bol- JSTOR, were searched for terms that included but were not len, 1996). It is likely that F. subglutinans plays a minor role limited to “asparagus miner,” “early decline,” “Fusarium in the North American FCRR (Elmer et al., 1996), as it is crown and root rot,” and “replant problem.” For the pur- less often isolated from asparagus plants (Vujanovic et al., pose of the ' gures and tallying, the term “experiments” 2006). In the United States, the primary pathogens associ- refers to individual experiments within studies, and it is ated with FCRR are considered to be F. proliferatum (teleo- possible to have more than one experiment dealing with morph Gibberella fujikuroi; Elmer, 1995) and F. oxysporum f. a similar subject within a study. A full meta-analysis of sp. asparagi, which primarily infects the crown–stem region the data in the reviewed articles was not possible because and roots, respectively (Van Bakel and Kerstens, 1970; Gor- of wide variability in dependent variables and treatments. don and Martyn, 1997). Fusarium oxysporum is implicated in However, when there was su( cient replication between infecting and causing FCRR in the root system of aspara- studies within a subject, nonparametric statistics (Mann– gus (Van Bakel and Kerstens, 1970), although it has also Whitney U tests) were used to evaluate di) erences in vari- been isolated from other parts of the asparagus plant (Tuell ables, since the assumptions of normality were not ful' lled. and Hausbeck, 2008). Fusarium oxysporum is thought to play a signi' cant role in newly planted ' elds, often hindering Biology, Biogeography, and Pathogenicity establishment of asparagus (Cohen and Heald, 1941; Gra- of Fusarium spp. ham, 1955; Endo and Burkholder, 1971), while F. prolifera- Since FCRR was ' rst described in 1908, Fusarium spp. have tum is thought to a) ect older ' elds and thereby plays a key undergone extensive taxonomic revision, having originally role in the early decline of asparagus. been described as F. moniliforme J. Sheld. (Snyder and Tous- soun, 1965; Proctor et al., 2010). In 1983, F. moniliforme was Symptoms, Severity, and Cost of Fusarium taxonomically split into F. proliferatum and F. subglutinans Crown and Root Rot (Nelson et al., 1983). On the other hand, F. oxysporum Wol- Fusarium crown and root rot of asparagus symptoms lenw. was originally identi' ed as one of the causal agents of include wilting, dwar' ng, chlorosis, browning of vascu- FCRR by Cohen and Heald (1941) and later grouped into lar tissue, death to the growing point, and damping o) formae speciales based on subsets of isolates that can infect in seedlings (Eskelsen and Schreiber, 1997; USDA, 1999). speci' c host crops (Snyder and Hansen, 1940; Grogan and The pathogen spreads basipetally toward the crown, often Kimble, 1959). However, F. oxysporum f. sp. asparagi may also causing premature plant death. Symptoms of infection be pathogenic to other crops, such as celery (Apium graveolens are usually observed during midsummer, and infection L.) and onion (Allium cepa L.) (Armstrong and Armstrong, with Fusarium spp. can also result in the complete destruc- 1969; Blok and Bollen, 1997; Elmer, 2001). Elmer (2001) has tion of the feeder roots and withering of the storage called the monophyletic status of F. oxysporum into question, roots (Elmer et al., 1996). Damage from FCRR can be and recent studies have shown that F. oxysporum is in fact exacerbated by exposure to viral agents including AV-1, polyphyletic and may not be a good biological species (Wong AV-2, and tobacco streak virus (Evans and Stephens, 1989; and Je) ries, 2006; for review, see Lievens et al., 2008). Kna* ewski et al., 2008), asparagus allelopathic residues

CROP SCIENCE, VOL. 51, JULY–AUGUST 2011 WWW.CROPS.ORG 1415 (Hartung and Stephens, 1983), environmental stress until mid-June, during which time the adults mate and the (Nigh, 1990), and insect damage (i.e., asparagus miner females oviposit on the asparagus stem near the soil surface damage, which serves as entry sites for Fusarium infection; (Fig. 1). The second generation begins to emerge at the Damicone et al., 1987). beginning of August and spans until around September The development of FCRR in asparagus plantings has (Ferro and Gilbertson, 1982; Lampert et al., 1984; Tuell negative economic impacts that include the loss of the ini- and Hausbeck, 2008). Adult populations can be sampled tial costs associated with establishing an asparagus planting, with yellow sticky traps (Ferro and Suchak, 1980). Tuell which is estimated to be more than $8600 ha−1 (J. Bakker, (2003) sampled for the asparagus miner with a regime that personal communication, 2010). Yields may be decreased involved canopy (1.5-m height) and ground (0.4 m high) by 2.22 to 3.03 kg ha–1 yr–1 when a planting is a) ected by traps with sticky traps deployed at each height. Canopy- FCRR (Reid et al., 2001). Currently, an asparagus ' eld level traps caught higher numbers of adults than ground- planted in Michigan is productive for approximately one- level traps (Tuell, 2003). half as much time as one that was planted in the 1950s, as Within the last several decades, damage from asparagus a result of FCRR and other pathogens such as Phytophthora miner has become recognized as a factor in exacerbating asparagi, as well as autotoxicity from asparagus residues (J. FCRR, despite long being considered unimportant after it Bakker and N. Myers, personal communication, 2010). was ' rst described (Dingler, 1934; Eichmann, 1943). Newly planted ' elds are quickly colonized by the asparagus miner The Biology and Role of the Asparagus (Tuell, 2003; Tuell and Hausbeck, 2008), with pathogenic Miner as a Vector Fusarium spp. occurring on the pupae, mines, and adults of The asparagus miner is a bivoltine organism (Ferro and Gil- asparagus miner (Gilbertson et al., 1985; Tuell and Haus- bertson, 1982; Lampert et al., 1984; Tuell, 2003), and its beck, 2008), as well as larvae and larval frass (Ferro and Gil- only known host is asparagus (Spencer, 1973). In the United bertson, 1982). In older ' elds, more than 25% and 20% of States, the asparagus miner occurs wherever asparagus is the pupae from the asparagus miner had evidence of spores grown, including the major asparagus-producing regions from F. proliferatum and F. oxysporum, respectively, on their of Washington (Eichmann, 1943), Michigan (Tuell, 2003), exterior. A total of 44% and 4% of stem tissue pieces from and California (Essig, 1913). The asparagus miner has also aboveground mines were colonized by F. proliferatum and F. been recorded from other asparagus-growing regions in the oxysporum, respectively (Tuell and Hausbeck, 2008). Larval world, including central Hungary, France, and Germany mining predisposes the upper stems of asparagus to Fusar- (Dingler, 1934). The asparagus miner was likely introduced ium infection, and the overwintering pupae serve as a form to the United States from Europe (Dingler, 1934; Spen- of inoculum of Fusarium spp. for the next growing season cer, 1973) when asparagus was brought to the New World (Ferro and Gilbertson, 1982). by French Huguenots (Scho' eld, 1946), despite being ' rst Increased incidence of the asparagus miner has been recorded from Pennsylvania in 1869 by H. Loew. linked to increased severity in FCRR infection in aspara- Adults of the asparagus miner oviposit on the stem of gus (Damicone et al., 1987) and decreased yields. High the asparagus near the soil surface, and once the eggs hatch, populations of asparagus miner may exacerbate FCRR, the larvae start producing mines and shafts in the cortex of resulting in decline of the asparagus yield until it is no the asparagus stems (Barnes, 1937). The damage from the longer pro' table to harvest. miner is considered to have a negligible e) ect on plant vigor (Dingler, 1934; Barnes, 1937; Eichmann, 1943). The aspar- Managing Fusarium Disease agus miner typically has two generations per season, and Most studies have focused on F. oxysporum (Fig. 2). There asparagus plantings may exhibit nearly 80 to 100% mining have been many attempts to limit FCRR through cultural, incidence in certain years (Tuell, 2003). In 2010, Michi- fungicidal, and biological control approaches, including gan experienced an unusually warm and extended grow- (i) using nonpathogenic Fusarium spp. (Reid et al., 2002); ing season, exacerbating miner activity and associated crop (ii) salting with NaCl (Reid et al., 2001; Elmer, 2004); damage, with a stem sometimes infested by more than six (iii) using arbuscular mycorrhizae (Counts and Hausbeck, asparagus miner pupae (R. Morrison, personal observation, 2008); (iv) incorporating asparagus root residues (Blok 2010). By contrast, the total number of pupae collected in a and Bollen, 1996); (v) performing biological soil disinfes- normal year (e.g., 2002) ranged from three to six per stem tation (Blok et al., 2008); (vi) using fungicides, including (Tuell, 2003) in the same area. These sites of damage pres- benomyl, thiophanate-methyl, and * udioxonil (Counts ent openings for pathogenic Fusarium spp. to gain access to and Hausbeck, 2008); (vii) employing antibiotics from the plant and cause FCRR (Ferro and Gilbertson, 1982). Streptomyces griseus (Smith et al., 1990); and (viii) devel- In Michigan, the asparagus miner overwinters as oping genetic resistance against Fusarium by gametophyte pupae in plant debris and the soil, with the ' rst generation selection (Pontaroli and Camadro, 2001). These measures emerging in May. The ' rst generation spans from May have exhibited varying levels of e( cacy (Table 1).

1416 WWW.CROPS.ORG CROP SCIENCE, VOL. 51, JULY–AUGUST 2011 Figure 1. Life cycle of the asparagus miner based on previously published research. Illustrated by Marlene Cameron. Of the examined experiments, the vast majority of et al., 2010). Advances in polymerase chain reaction–based them target F. oxysporum (Fig. 2). There are very few stud- (Yergeau et al., 2005) and genomics methods make it pos- ies that have speci' cally looked at F. proliferatum, the main sible to correctly identify F. proliferatum and F. oxysporum by agent currently implicated in the early decline of aspara- using calmodulin gene sequences (Mule et al., 2004). gus. This is likely due to the high degree of morphological The most extensively examined management prac- similarity between F. proliferatum and F. oxysporum (Proctor tices include salting, and the use of nonpathogenic Fusar- ium spp. to compete with pathogenic Fusarium spp. Salting with NaCl is signi' cantly better than employing nonpathogenic Fusarium species (Mann–Whitney U test: U = 0, P < 0.0199). Salting used to be standard practice among asparagus growers to control weeds in the 19th and beginning of the 20th centuries (Elmer et al., 1996), but fell into disuse with the advent of modern herbicides to counter weeds. The long-term consequences from salting ' elds may be a change in soil pH, salinity, and other parameters important for the yield of asparagus plantings (Hodupp, 1983). Reid et al. (2001) found that two annual applications of NaCl to a commercial production ' eld in Michi- gan did not signi' cantly a) ect levels of pH, potassium, magnesium, or calcium, nor did it increase the salinity in the soil from 15 cm. However, NaCl applications did Figure 2. Number of experiments in managing Fusarium species increase salinity in the soil to 5.4 mS m–1 in a deeper (15–30 reviewed in this paper. Experiments attempting to control F. cm) layer. Most studies where NaCl successfully reduced oxysporum are overrepresented relative to F. proliferatum. Foa = FCRR severity were conducted in greenhouses, growth F. oxysporum, Fp = F. proliferatum, Fma = F. moniliforme, Fr = chambers, or small ' eld plots. The ' eld-plot research was F. redolens.

CROP SCIENCE, VOL. 51, JULY–AUGUST 2011 WWW.CROPS.ORG 1417 conducted in severely declined asparagus plantings of a revealed that mesotrione can be phytotoxic to asparagus small, noncommercial scale and may not represent larger and could result in decreased yields (Rodriguez-Sal- commercial production ' elds. When commercial ' eld amanca, 2010). Future research should investigate the trials with salt were conducted in Michigan, there was e) ect that certain management regimes (including herbi- no increase in the yield of asparagus (Reid et al., 2001). cides) have on asparagus plant vigor and the progression In addition, NaCl exacerbates Phytophthora crown and of FCRR. Overall, an e) ective strategy for combating root rot, which is recognized as an important pathogen FCRR should include a multipronged approach that of asparagus in Michigan (Saude et al., 2008) and Cali- includes fungicides, continuing selection for resistance fornia (Falloon et al., 1991). As a result of these combined against Fusarium spp., and certain cultural techniques such factors, salting is not a recommended strategy to control as avoiding herbicides that are phytotoxic to asparagus and Fusarium spp. irrigation to avoid environmental stress in asparagus. Another cultural method that has been investigated is biological soil disinfestation (Table 1; Blok et al., 2008), Controlling Asparagus Miner Populations which has been used to manage F. redolens Wollenw., with The asparagus miner remains an understudied species, positive results. This process requires growers to dig up to especially considering its role as a putative vector in the 80 cm in the ground to deposit grass clippings and subse- spread of FCRR in asparagus ' elds. Repeated applica- quently to cover the entire ' eld in airtight plastic. Because tions of the insecticide diazinon after the harvesting this method has not been attempted for other species of season reduced asparagus miner incidence and severity Fusarium and is labor intensive, more research is needed of FCRR, and increased yield (Damicone et al., 1987). before any conclusive recommendations can be made. An action threshold has not been established for timing Biological control has also been investigated as a means insecticide applications that target the asparagus miner, to manage FCRR. This has been performed using non- presenting added di( culty. Although a sampling regime pathogenic Fusarium spp. (Blok and Bollen, 1996; Elmer, for the asparagus miner that uses canopy-level sticky traps 2004; Counts and Hausbeck, 2008). has been shown to help (Tuell, 2003), sticky traps are not Much prior investment has been directed to develop- species speci' c, and can therefore be time-consuming to ing Fusarium-resistant asparagus cultivars (e.g., Stephens process. A sampling regime that uses fewer traps, or a trap et al., 1989; Dan, 1994; Dan and Stephens, 1995; He et with a species-speci' c lure, may increase the e( ciency of al., 2002; He and Wolyn, 2005). However, this has not monitoring asparagus miner populations. yielded a viable commercial cultivar. A promising long- It is important to utilize IPM strategies to reduce reli- term approach to combat FCRR involves gametophyte ance on insecticides and to manage populations of aspara- selection of asparagus plants resistant to Fusarium spp. gus miner. One method is to incorporate biological control (Pontaroli et al., 2000; Pontaroli and Camadro, 2001). into a management regime for the asparagus miner, but there Select fungicides, fumigants, and an antibiotic signi' - has only been limited research on the parasitoids of the spe- cantly reduced FCRR, particularly thiophanate-methyl, cies. In the United Kingdom, Giard (1904 c.f. Barnes, 1937) metam-potassium, Telone C-35 (Dow AgroSciences, Indi- described a parasitoid, Dacnusa rondanii Giard (Hymenoptera: anapolis, IN), and faeriefungin (Table 1). Fungicides and Braconidae), on asparagus miner. About three decades later, fumigants have not been widely used to reduce FCRR, also in the United Kingdom, Barnes (1937) described three but ' eld trials are ongoing (Hausbeck and Cortright, 2008). additional hymenopteran parasitoids of the asparagus miner: Further development and testing of fungicidal compounds Pediobius epigonus (Walker) (Eulophidae; formerly Pleurotro- targeting Fusarium spp. would bene' t growers. pis epigonus; Spencer, 1973), Sphegigaster sp. (Pteromalidae), Stress is an important factor in promoting FCRR in and misidenti' ed Chorebus rondanii (Giard) (Braconidae) asparagus (Nigh, 1990). Sandy soils, which are predominant as Dacnusa bathyzona Marshall (Gri( ths, 1967). However, in many asparagus-growing regions, especially in Michi- none of these biological control agents were evaluated for gan, are very porous and do not retain water, which may their e( cacy, nor have any parasitoids been described in the lead to water stress conditions for asparagus ' elds. Research United States. This aspect of research provides potential for into irrigation methods and timing to reduce environmen- the future management of both the asparagus miner and the tal stress for asparagus could reduce FCRR severity. associated FCRR. Asparagus growers rely on herbicides for weed con- Semiochemicals are chemicals emitted from plants or trol, especially in young plantings. Growers have become insects that may be used as a tool in an IPM program concerned with speci' c herbicides and their observed to manage the asparagus miner. To our knowledge, there negative e) ects on asparagus fern growth. Greenhouse have been no studies on the response of the asparagus trials were conducted to evaluate the e) ect of select herbi- miner to the volatiles of asparagus. If compounds that are cides on asparagus growth, and the application of mesot- attractive to the asparagus miner are identi' ed, these could rione resulted in a reduction in crown weight. Field trials

1418 WWW.CROPS.ORG CROP SCIENCE, VOL. 51, JULY–AUGUST 2011 (cont’d) 2001 2008 2008 Elmer, 2004Elmer, Elmer, 2008Elmer, 2008Elmer, Reid 2001 et al., Reid 2001 et al., Reid 2001 et al., Reid 2001 et al., Reid 2001 et al., Pontaroli and Camadro, NS Reid 2001 et al., stalks > 0.79 cmstalks > 0.79 root lesions from Foa root lesions from Foa root lesions from Foa 9.5% better9.5% stand count Counts and Hausbeck, marketable spear weights 13% increase13% in the no. of NS increase in root weight rootarea for certain crosses 16% increase16% in root weight 7% reduction7% in root lesions 2008 Elmer, from and Fp, NS decrease in g more fresh weight per plant 12% increase12% in the 3-yr total 35% decrease35% in root lesions, 11.6% increase in root lesions11.6% 39% decrease in root lesions, 27.4% decrease in root lesions27.4% 14.8% decrease14.8% in root lesions from Fp, and 16.1% increase in from and Fp, 16.1% 28.4–45.8% decrease in FCRR Blok 2008 et al., 15.3% decrease in root rot, 0.55 0.55 rot, decreaseroot in 15.3% from Fp, and 33.1% decrease in from and Fp, 33.1% 3.78–10.34% decrease in affected affected in decrease 3.78–10.34% NS NS Blok and Bollen, 1996 FCRR FCRR FCRR Change in condition Citations in FCRR in FCRR in FCRR in FCRR measured stand count cacy against Signifi cant and Signifi strong reduction increase in FCRR Effi reduction in FCRR reduction in FCRR reduction in FCRR Signifi cant reduction Signifi Signifi cant reduction Signifi Signifi cant and strong Signifi § with Foa to 6% TCF 6% to residues added Salting drench once after planting Cultural practices and covered with airtight plastic colonization, applied as 100-mL Greenhouse Cl equivalent other to treatmentscant reduction Signifi Greenhouse Cl equivalent other to treatmentsGreenhouse NS Cl equivalent other to treatmentsGreenhouse Cl equivalent other to treatments NS NSGreenhouse NS Sterilized asparagus root NS Reid 2001 et al., NSGreenhouse Reid 2001 et al., Controlled crosses exposed Reid 2001 et al., Research fi eld Research fi Applied three times during April No direct measure of Abandoned fi eld Abandoned fi Grass added at 80-cm soil depth Commercial fi eld Commercial fi Addition by crown dip or irrigationeld Commercial fi NS Addition by crown dip or irrigationcant better Signifi NSeld Commercial fi Applied in the spring Counts and Hausbeck, No direct measure of Commercial fi eld Commercial fi Applied three times during April NS NS Reid 2001 et al., –1 –1 –1 OO Greenhouseavone that promotes AM fungi Isofl eld Research fi eld Soaked for 20 min in fi FCRR not directly –1 –1 –1 2 2 O Greenhouse mL applied 100 1 wk after plantingcant reduction Signifi –1 –1 –1 –1 2 − 1 H H H –1 –1 or 1.57 g L or 1.57 –1 –1 –1 m or row- g 55.6 –1 Amount Type Description † Fr t ha 62–102 Foa L kg 0.02 Foa and FpFoa and Fp mM 17.1 g pot 0.40 Growth chamber Cl equivalent other to treatmentsFoa and Fpcant and strong Signifi Foa and Fp 8.55 mM 0.53 g pot Growth chamber Cl equivalent other to treatments NS NS Reid 2001 et al., strategy Target Management 2 2 2 2 fungi addition Foa mL plant 1.2 ClCl Foa and Fp Foa and Fp 34.2 mM 0.29 g pot Growth chamber Cl equivalent other to treatmentscant and strong Signifi ‡ 4 4 Formononetin Foa mg 20 L NaClCaCl NH Foa and Fp mM 17.1–34.2 MnCl MnCl Growth chamber Cl equivalent other to treatmentscant and strong Signifi Trichoderma harzianum Table 1. Overview 1. Table of different techniques used control to Fusarium crown and root rot (FCRR). NaClNaCl Foa Foa and Fp g L 10 ha kg 1120 Lime Foa and Fp ha kg 6719 AM NH Biological soil disinfestation Root residueFormononetin Foa Foa kg g 20 mg 20 L NaClNaCl Foa Foa and Fp NaCl 1% g pot 0.32 Greenhouse Added mL 100 after infection Gametophyte selection Foa 50–200 seeds treatment CaCl NaCl Foa and Fp ha kg 560–1120

CROP SCIENCE, VOL. 51, JULY–AUGUST 2011 WWW.CROPS.ORG 1419 (cont’d) 2008 2008 2008 2008 Elmer, 2004Elmer, Elmer, 2004Elmer, 2004Elmer, 2004Elmer, 2004Elmer, Elmer, 2008Elmer, Hausbeck 2006 et al., Hausbeck 2006 et al., Hausbeck 2006 et al., –1 − 1 g soil ¶ CFU g soil CFU weight without NaCl decrease in disease rating disease in decrease 25.6% better25.6% stand count Counts and Hausbeck, 27.3% greater root weight 27.3% marketable spear weights marketable spear weights decrease in disease rating disease in decrease 8% reduction8% in root lesions 2008 Elmer, ft) and 3.3 cm greater height NS increase in stand counts, 12% increase12% in the 3-yr total 10% reduction10% in root lesions 2004 Elmer, 36% increase in the 3-yr total with NaCl, 16.7% greaterwith root NaCl, 16.7% 18.5 more m (20 ferns18.5 per 6.1 Reduced Foa and by 1520 Fp Reduced Foa and by 1620 Fp NS decrease in disease rating NS decrease in root lesions, NS lesions, root in decrease NS increase in stand counts, 13.8% 13.8% counts, stand in increase NS decrease in root lesions, NS increase in stand counts, 15.4% NSNS NS NS Counts and Hausbeck, Counts and Hausbeck, FCRR Change in condition Citations in vigor in FCRR in FCRR in FCRR in FCRR in FCRR in FCRR measured measured root weight cacy against stand condition Effi Signifi cant reduction Signifi Signifi cant reduction Signifi depth once depth once or irrigation trial or irrigation trial Cultivars Fungicides Nonpathogenic Fusarium GreenhouseGreenhouse Roots of plants soaked in 500 mL Roots of plants soaked in 500 mL NSGreenhouse NSGreenhouse Roots of plants soaked in 500 mL Roots of plants soaked in 500 mLcant reduction Signifi NS NSGreenhouse NS Roots of plants soaked in 500 mLcant increase in Signifi Greenhouse Roots of plants soaked in 500 mLcant reduction NS Signifi 2004 Elmer, 2004 Elmer, Greenhouse Roots of plants soaked in 500 mL 2004 Elmer, NS NS 2004 Elmer, Research fi eld Research fi Shank-applied 30-cm at 25- to Research fi eld Research fi Crowns dipped L for 20 min in 10 NSeld Research fi eld Researcheld fi Soaked for 20 min in fi NS decrease in root lesions, Crowns dipped L for 20 min in 10 cant decrease Signifi FCRR not directly eld Research fi eld Researcheld fi Soaked for 20 min in fi Crowns dipped L for 20 min in 10 cant decrease Signifi FCRR not directly eld Research fi Shank-applied 30-cm at 25- to Commercial fi eld Commercial fi Addition by crown dip or irrigation NS NS Counts and Hausbeck eld Commercial fi Fungicide addition by crown drip eld Commercial fi Fungicide addition by crown dripeld Commercial fi cant better Signifi Fungicide addition by crown drip eld Commercial fi Crown soakcant increase Signifi –1

–1 –1 –1 − 1 − 1 ) ) –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 –1 or = 144eld Research ﬁ Nonresistant cultivar NS NS Damicone 1987 et al., –1 –1 –1 N or 5.67 g 30.5 or 5.67 spores mL spores mL spores mL 5 5 5 or 76.5 kg ha kg or 76.5 row-m –1 Amount Type Description spores mL spores mL spores mL spores mL spores mL spores mL spores mL spores mL spores mL –1 4 4 4 4 4 4 4 4 4 397 g 12 m g 12 397 (227.1 L acre (227.1 (132.5 L acre L (132.5 = 288 or N † Foa ha kg 427

Fusarium strategy Target Management CS-20 Foa 10 Telone C-35Telone Cannonball 50WP Foa and Fp Foa and Fp L 0.404 ha 132.5 L g 378.5 14.2 CWB 314CWB 314CWB 318CWB 318 Foa Foa 10 5 × 10 Foa Foa 10 CS-20 10 FoaThiophanate-methyl 10 Metam-potassium Foa Foa and Fp g L 1.20 L 0.404 ha 227.1 Table 1. Continued. 1. Table CWB 318CWB 318 FoaCS-20 10 Foa 5 × 10 FoaFO47 10 Foa 10 Nonpathogenic spp. CWB 312 Foa 10 ‘Mary Washington’Benomyl Fma and Foa Fludioxonil Foa g L 1.20 Foa g L 0.6 CS-20 Foa 5 × 10

1420 WWW.CROPS.ORG CROP SCIENCE, VOL. 51, JULY–AUGUST 2011 potentially be used for baits in traps, making population sampling more precise and e) ective. Research is also needed on the identi' cation of source populations of asparagus miner in new plantings of asparagus. It is not known where asparagus miner populations

Smith 1990 et al., originate and if they use alternative hosts; it is assumed Damicone 1987 et al., that they come from volunteer asparagus plants (N. Myers, personal communication, 2010). The types of habitats or , and vegetation outside production ' elds that harbor the asparagus miner should be identi' ed and methods pursued to suppress immigrating populations.

increase in yield CONCLUSIONS AND FUTURE RESEARCH Ophiomyia simplex

dry ﬁ brous root weight dry ﬁ There are >250,000 ha of asparagus globally (Benson, nal stem rot index and mines from 36-mm increase in asparagus Decrease in external and inter- shoot length, increase 133% in 2009), representing a major investment of economic resources. Fusarium crown and root rot is a signi' cant barrier to increased productivity. Moreover, FCRR is a di( cult disease to manage and therefore e) orts to date have focused on exclusion of the pathogen via soil fumi- FCRR Change in condition Citations and mines

cacy against gation of seedling nurseries, crown fungicidal soaks, and Effi reduction in FCRR reduction in FCRR cultural strategies, including a neutral pH of the soil, no Signifi cant and strong Signifi Signifi cant and strong Signifi tillage, and other horticultural techniques (e.g., no over- picking) to enhance plant vigor. Due to the link between FCRR and the asparagus miner, it is necessary to address each. An IPM strategy is needed to address the following: (i) the role of semiochemicals in attracting asparagus miner to asparagus, and the pheromones driving mating behavior; (ii) identifying habitats that act as reservoirs of asparagus Streptomyces griseus by insectby activity Antibiotics Herbicides

Insecticides miner for newly planted ' elds; (iii) identifying and increasing the e( cacy of natural enemies of the asparagus miner; (iv) developing an economic threshold for pesticide appli-

. cation to guide management of the asparagus miner; (v) alleviating human-induced plant damage (e.g., the impact of speci' c herbicides weakening the asparagus crown and

F. moniliformeF. making it more vulnerable); (vi) using cultural techniques Research fi eld Research fi eld Research fi Sprayed when warranted Fumigated in falleld Research fi Sprayed beginning of season NS NS NS NS Damicone 1987 et al., Damicone 1987 et al., Growth chamber From to reduce natural stresses to asparagus; and (vii) delivering

; Fma; = e) ective pesticides and fungicides via drip irrigation to the –1 root zone. A program that results from research advances –1 –1 –1 will manage asparagus miner and FCRR in a cost-e) ective

F. redolensF. manner with minimal impact on ecosystems. Amount Type Description ; Fr = = Fr ; (12.5–50 ppm) (12.5–50 Acknowledgments W.R.M. is funded by the C.S. Mott Predoctoral Fellowship in Sustainable Agriculture and a grant from MSUE-Project F. proliferatumF. † GREEEN (GR10-052). ; Fp = = Fp ; References Armstrong, G.M., and J.K. Armstrong. 1969. Relationships of asparagi Fusarium oxysporum formae specialis apii, asparagi, cassiae, mel- f. sp. f. ongenae, and vasinfectum race 3 as revealed by pathogenicity for common hosts. Phytopathology 59:1256–1260. Barnes, H.F. 1937. The asparagus miner (Melanagromyza simplex H.

strategy Target Loew) (Agromyzidae; Diptera). Ann. Appl. Biol. 24:574–588. F. oxysporumF.

Management doi:10.1111/j.1744-7348.1937.tb05854.x Benson, B.L. 2009. 2009 update on the world’s asparagus CFU colony-forming = units. Foa = AM = arbuscular mycorrhizae. ltrate. TCF toxic = culture ﬁ Vorlex Fma and Foa 363 L ha Simazine Fma and Foa 6.20 ha kg Table 1. Continued. 1. Table Diazinon† Fma and Foa‡ § ¶ ha 0.63 kg Faeriefungin Foa mg 12.49–49.94 L

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