constraints on asparagus production: the association of ophiomyia

1414 WWW.CROPS.ORG CROP SCIENCE, VOL. 51, JULY–AUGUST 2011

REVIEW & INTERPRETATION

Asparagus (Asparagus o! cinalis L.) production has become increasingly constrained globally during the past several

decades because of problems with replanting asparagus ' elds and the early onset of asparagus stand decline (Grogan and Kimble, 1959; Elmer et al., 1996). Grogan and Kimble (1959, p. 122) de' ned asparagus decline as “a slow decline in the productiv-ity of old asparagus plantings … to the point where the plant-ings become unpro' table to maintain.” The authors furthermore de' ned the replant problem as “the inability to establish produc-tive plantings … where plantings have declined” (Grogan and Kimble, 1959, p. 122). Early decline of asparagus can lead to a reduction in the lifespan of planted ' elds by 5 to 8 yr; farmers are not able to recoup the investment associated with establishing asparagus ' elds (Elmer et al., 1996).

The fungi Fusarium subglutinans Wollenw. & Reinking, Fusar-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 inabil-ity 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

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

ABSTRACTProduction of asparagus (Asparagus offi cinalis L.) is globally constrained by the “early decline” syndrome. The primary causal agents of early decline include Fusarium proliferatum (Matsu-shima) Nirenberg, F. oxysporum Wollenw. f. sp. asparagi S.I. Cohen, and F. subglutinans Wol-lenw. & Reinking. These pathogens together contribute to Fusarium crown and root rot (FCRR). Damage to asparagus stems, especially by the asparagus miner (Ophiomyia simplex Loew [Diptera: Agromyzidae]), has been associ-ated with and shown to exacerbate FCRR. This review synthesizes the current information on this tripartite interaction, describes manage-ment strategies and their ef! cacy, and high-lights needed research. Opportunities for future control of the asparagus miner and associated FCRR are presented. Research areas of interest include investigating the role of semiochemicals in the asparagus miner–Fusarium spp. interac-tion, identifying effective biological controls for the asparagus miner, and determining source populations of asparagus miner in new aspara-gus plantings.

W.R. Morrison III, J.K. Tuell, and Z. Szendrei, Dep. of Entomology, Michigan State Univ., 243 Natural Science, East Lansing, MI 48824-1311; M.K. Hausbeck, Dep. of Plant Pathology, Michigan State Univ., 107 Center for Integrated Plant Systems, East Lansing, MI 48824-1115. Received 14 Feb. 2011. *Corresponding author ([email protected]).

Abbreviations: FCRR, Fusarium crown and root rot; IPM, inte-grated pest management.

Published in Crop Sci. 51:1414–1423 (2011).doi: 10.2135/cropsci2011.01.0032Published 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.

CROP SCIENCE, VOL. 51, JULY–AUGUST 2011 WWW.CROPS.ORG 1415

was last grown (Poll and Huiskamp, 1992). The asparagus miner, Ophiomyia simplex Loew (Diptera: Agromyzidae), acts as a putative vector for infection of asparagus plants with Fusarium. The larvae cause damage to the plant (Tuell and Hausbeck, 2008), exacerbating the early decline of asparagus ' elds (Gilbertson et al., 1985).

The purpose of this review is to examine and synthe-size the current information about this tripartite interac-tion between asparagus, the Fusarium spp. associated with Fusarium crown and root rot (FCRR), and the asparagus miner. We examine potential methods to limit the aspara-gus miner and thereby reduce FCRR, and discuss future research areas, including the need for an integrated pest management (IPM) approach.

METHODSThis review is a synthesis of information regarding FCRR and the asparagus miner. The Michigan State University library collection and online databases, including Web of Science, ScienceDirect, SpringerLink, Google Scholar, and JSTOR, were searched for terms that included but were not limited to “asparagus miner,” “early decline,” “Fusarium crown and root rot,” and “replant problem.” For the pur-pose of the ' gures and tallying, the term “experiments” refers to individual experiments within studies, and it is possible to have more than one experiment dealing with a similar subject within a study. A full meta-analysis of the data in the reviewed articles was not possible because of wide variability in dependent variables and treatments. However, when there was su( cient replication between studies within a subject, nonparametric statistics (Mann–Whitney U tests) were used to evaluate di) erences in vari-ables, since the assumptions of normality were not ful' lled.

Biology, Biogeography, and Pathogenicity of Fusarium spp.Since FCRR was ' rst described in 1908, Fusarium spp. have undergone extensive taxonomic revision, having originally been described as F. moniliforme J. Sheld. (Snyder and Tous-soun, 1965; Proctor et al., 2010). In 1983, F. moniliforme was taxonomically split into F. proliferatum and F. subglutinans (Nelson et al., 1983). On the other hand, F. oxysporum Wol-lenw. was originally identi' ed as one of the causal agents of FCRR by Cohen and Heald (1941) and later grouped into formae speciales based on subsets of isolates that can infect speci' c host crops (Snyder and Hansen, 1940; Grogan and Kimble, 1959). However, F. oxysporum f. sp. asparagi may also be pathogenic to other crops, such as celery (Apium graveolens L.) and onion (Allium cepa L.) (Armstrong and Armstrong, 1969; Blok and Bollen, 1997; Elmer, 2001). Elmer (2001) has called the monophyletic status of F. oxysporum into question, and recent studies have shown that F. oxysporum is in fact polyphyletic and may not be a good biological species (Wong and Je) ries, 2006; for review, see Lievens et al., 2008).

Fusarium spp. are anamorphic (Gordon and Martyn, 1997) and nearly ubiquitous in both agricultural soils and native soils around the world (Hartung et al., 1990; Vuja-novic et al., 2006). Both pathogenic and nonpathogenic strains of Fusarium spp. can be found in soils, even those that have not been planted to asparagus (Hartung et al., 1990). Fusarium oxysporum may infect young feeder roots, gaining entry at the junction where the feeder roots emerge (Gra-ham, 1955; Smith and Peterson, 1983) between epidermal cells. Subsequently, the fungus moves into the cells, radiating intercellularly into the cortex of the root. Lesions that are small, red, and elliptical develop on the feeder root tips and along the root (Shoemaker, 1965 cf. Elmer, 2001), and may also be evident on the underground portion of the plant stem. Asparagus that is damaged or stressed from cultural practices or other means is more susceptible to FCRR (Nigh, 1990).

Di) erent species of Fusarium are found in varying regions in the world: for example, in the Netherlands, F. culmorum (W.G. Sm.) Sacc. is associated with FCRR, while F. proliferatum and F. oxysporum are absent (Blok and Bol-len, 1996). It is likely that F. subglutinans plays a minor role in the North American FCRR (Elmer et al., 1996), as it is less often isolated from asparagus plants (Vujanovic et al., 2006). In the United States, the primary pathogens associ-ated with FCRR are considered to be F. proliferatum (teleo-morph Gibberella fujikuroi; Elmer, 1995) and F. oxysporum f. sp. asparagi, which primarily infects the crown–stem region and roots, respectively (Van Bakel and Kerstens, 1970; Gor-don and Martyn, 1997). Fusarium oxysporum is implicated in infecting and causing FCRR in the root system of aspara-gus (Van Bakel and Kerstens, 1970), although it has also been isolated from other parts of the asparagus plant (Tuell and Hausbeck, 2008). Fusarium oxysporum is thought to play a signi' cant role in newly planted ' elds, often hindering establishment of asparagus (Cohen and Heald, 1941; Gra-ham, 1955; Endo and Burkholder, 1971), while F. prolifera-tum is thought to a) ect older ' elds and thereby plays a key role in the early decline of asparagus.

Symptoms, Severity, and Cost of Fusarium Crown and Root RotFusarium crown and root rot of asparagus symptoms include wilting, dwar' ng, chlorosis, browning of vascu-lar tissue, death to the growing point, and damping o) in seedlings (Eskelsen and Schreiber, 1997; USDA, 1999). The pathogen spreads basipetally toward the crown, often causing premature plant death. Symptoms of infection are usually observed during midsummer, and infection with Fusarium spp. can also result in the complete destruc-tion of the feeder roots and withering of the storage roots (Elmer et al., 1996). Damage from FCRR can be exacerbated by exposure to viral agents including AV-1, AV-2, and tobacco streak virus (Evans and Stephens, 1989; Kna* ewski et al., 2008), asparagus allelopathic residues


until mid-June, during which time the adults mate and the females oviposit on the asparagus stem near the soil surface (Fig. 1). The second generation begins to emerge at the beginning of August and spans until around September (Ferro and Gilbertson, 1982; Lampert et al., 1984; Tuell and Hausbeck, 2008). Adult populations can be sampled with yellow sticky traps (Ferro and Suchak, 1980). Tuell (2003) sampled for the asparagus miner with a regime that involved canopy (1.5-m height) and ground (0.4 m high) traps with sticky traps deployed at each height. Canopy-level traps caught higher numbers of adults than ground-level traps (Tuell, 2003).

Within the last several decades, damage from asparagus miner has become recognized as a factor in exacerbating FCRR, despite long being considered unimportant after it was ' rst described (Dingler, 1934; Eichmann, 1943). Newly planted ' elds are quickly colonized by the asparagus miner (Tuell, 2003; Tuell and Hausbeck, 2008), with pathogenic Fusarium spp. occurring on the pupae, mines, and adults of asparagus miner (Gilbertson et al., 1985; Tuell and Haus-beck, 2008), as well as larvae and larval frass (Ferro and Gil-bertson, 1982). In older ' elds, more than 25% and 20% of the pupae from the asparagus miner had evidence of spores from F. proliferatum and F. oxysporum, respectively, on their exterior. A total of 44% and 4% of stem tissue pieces from aboveground mines were colonized by F. proliferatum and F. oxysporum, respectively (Tuell and Hausbeck, 2008). Larval mining predisposes the upper stems of asparagus to Fusar-ium infection, and the overwintering pupae serve as a form of inoculum of Fusarium spp. for the next growing season (Ferro and Gilbertson, 1982).

Increased incidence of the asparagus miner has been linked to increased severity in FCRR infection in aspara-gus (Damicone et al., 1987) and decreased yields. High populations of asparagus miner may exacerbate FCRR, resulting in decline of the asparagus yield until it is no longer pro' table to harvest.

Managing Fusarium DiseaseMost studies have focused on F. oxysporum (Fig. 2). There have been many attempts to limit FCRR through cultural, fungicidal, and biological control approaches, including (i) using nonpathogenic Fusarium spp. (Reid et al., 2002); (ii) salting with NaCl (Reid et al., 2001; Elmer, 2004); (iii) using arbuscular mycorrhizae (Counts and Hausbeck, 2008); (iv) incorporating asparagus root residues (Blok and Bollen, 1996); (v) performing biological soil disinfes-tation (Blok et al., 2008); (vi) using fungicides, including benomyl, thiophanate-methyl, and * udioxonil (Counts and Hausbeck, 2008); (vii) employing antibiotics from Streptomyces griseus (Smith et al., 1990); and (viii) devel-oping genetic resistance against Fusarium by gametophyte selection (Pontaroli and Camadro, 2001). These measures have exhibited varying levels of e( cacy (Table 1).

(Hartung and Stephens, 1983), environmental stress (Nigh, 1990), and insect damage (i.e., asparagus miner damage, which serves as entry sites for Fusarium infection; Damicone et al., 1987).

The development of FCRR in asparagus plantings has negative economic impacts that include the loss of the ini-tial costs associated with establishing an asparagus planting, which is estimated to be more than $8600 ha−1 ( J. Bakker, personal communication, 2010). Yields may be decreased by 2.22 to 3.03 kg ha–1 yr–1 when a planting is a) ected by FCRR (Reid et al., 2001). Currently, an asparagus ' eld planted in Michigan is productive for approximately one-half as much time as one that was planted in the 1950s, as a result of FCRR and other pathogens such as Phytophthora asparagi, as well as autotoxicity from asparagus residues ( J. Bakker and N. Myers, personal communication, 2010).

The Biology and Role of the Asparagus Miner as a VectorThe asparagus miner is a bivoltine organism (Ferro and Gil-bertson, 1982; Lampert et al., 1984; Tuell, 2003), and its only known host is asparagus (Spencer, 1973). In the United States, the asparagus miner occurs wherever asparagus is grown, including the major asparagus-producing regions of Washington (Eichmann, 1943), Michigan (Tuell, 2003), and California (Essig, 1913). The asparagus miner has also been recorded from other asparagus-growing regions in the world, including central Hungary, France, and Germany (Dingler, 1934). The asparagus miner was likely introduced to the United States from Europe (Dingler, 1934; Spen-cer, 1973) when asparagus was brought to the New World by French Huguenots (Scho' eld, 1946), despite being ' rst recorded from Pennsylvania in 1869 by H. Loew.

Adults of the asparagus miner oviposit on the stem of the asparagus near the soil surface, and once the eggs hatch, the larvae start producing mines and shafts in the cortex of the asparagus stems (Barnes, 1937). The damage from the miner is considered to have a negligible e) ect on plant vigor (Dingler, 1934; Barnes, 1937; Eichmann, 1943). The aspar-agus miner typically has two generations per season, and asparagus plantings may exhibit nearly 80 to 100% mining incidence in certain years (Tuell, 2003). In 2010, Michi-gan experienced an unusually warm and extended grow-ing season, exacerbating miner activity and associated crop damage, with a stem sometimes infested by more than six asparagus miner pupae (R. Morrison, personal observation, 2010). By contrast, the total number of pupae collected in a normal year (e.g., 2002) ranged from three to six per stem (Tuell, 2003) in the same area. These sites of damage pres-ent openings for pathogenic Fusarium spp. to gain access to the plant and cause FCRR (Ferro and Gilbertson, 1982).

In Michigan, the asparagus miner overwinters as pupae in plant debris and the soil, with the ' rst generation emerging in May. The ' rst generation spans from May


Of the examined experiments, the vast majority of them target F. oxysporum (Fig. 2). There are very few stud-ies that have speci' cally looked at F. proliferatum, the main agent currently implicated in the early decline of aspara-gus. This is likely due to the high degree of morphological similarity between F. proliferatum and F. oxysporum (Proctor

et al., 2010). Advances in polymerase chain reaction–based (Yergeau et al., 2005) and genomics methods make it pos-sible to correctly identify F. proliferatum and F. oxysporum by using calmodulin gene sequences (Mule et al., 2004).

The most extensively examined management prac-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 non-pathogenic 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 begin-ning 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 applica-tions 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 increase salinity in the soil to 5.4 mS m–1 in a deeper (15–30 cm) layer. Most studies where NaCl successfully reduced FCRR severity were conducted in greenhouses, growth chambers, or small ' eld plots. The ' eld-plot research was

Figure 1. Life cycle of the asparagus miner based on previously published research. Illustrated by Marlene Cameron.

Figure 2. Number of experiments in managing Fusarium species reviewed in this paper. Experiments attempting to control F. oxysporum are overrepresented relative to F. proliferatum. Foa = F. oxysporum, Fp = F. proliferatum, Fma = F. moniliforme, Fr = F. redolens.


conducted in severely declined asparagus plantings of a small, noncommercial scale and may not represent larger commercial production ' elds. When commercial ' eld trials with salt were conducted in Michigan, there was no increase in the yield of asparagus (Reid et al., 2001). In addition, NaCl exacerbates Phytophthora crown and root rot, which is recognized as an important pathogen of asparagus in Michigan (Saude et al., 2008) and Cali-fornia (Falloon et al., 1991). As a result of these combined factors, salting is not a recommended strategy to control Fusarium spp.

Another cultural method that has been investigated is biological soil disinfestation (Table 1; Blok et al., 2008), which has been used to manage F. redolens Wollenw., with positive results. This process requires growers to dig up to 80 cm in the ground to deposit grass clippings and subse-quently to cover the entire ' eld in airtight plastic. Because this method has not been attempted for other species of Fusarium and is labor intensive, more research is needed before any conclusive recommendations can be made.

Biological control has also been investigated as a means to manage FCRR. This has been performed using non-pathogenic Fusarium spp. (Blok and Bollen, 1996; Elmer, 2004; Counts and Hausbeck, 2008).

Much prior investment has been directed to develop-ing Fusarium-resistant asparagus cultivars (e.g., Stephens et al., 1989; Dan, 1994; Dan and Stephens, 1995; He et al., 2002; He and Wolyn, 2005). However, this has not yielded a viable commercial cultivar. A promising long-term approach to combat FCRR involves gametophyte selection of asparagus plants resistant to Fusarium spp. (Pontaroli et al., 2000; Pontaroli and Camadro, 2001).

Select fungicides, fumigants, and an antibiotic signi' -cantly reduced FCRR, particularly thiophanate-methyl, metam-potassium, Telone C-35 (Dow AgroSciences, Indi-anapolis, IN), and faeriefungin (Table 1). Fungicides and fumigants have not been widely used to reduce FCRR, but ' eld trials are ongoing (Hausbeck and Cortright, 2008). Further development and testing of fungicidal compounds targeting Fusarium spp. would bene' t growers.

Stress is an important factor in promoting FCRR in asparagus (Nigh, 1990). Sandy soils, which are predominant in many asparagus-growing regions, especially in Michi-gan, are very porous and do not retain water, which may lead to water stress conditions for asparagus ' elds. Research into irrigation methods and timing to reduce environmen-tal stress for asparagus could reduce FCRR severity.

Asparagus growers rely on herbicides for weed con-trol, especially in young plantings. Growers have become concerned with speci' c herbicides and their observed negative e) ects on asparagus fern growth. Greenhouse trials were conducted to evaluate the e) ect of select herbi-cides on asparagus growth, and the application of mesot-rione resulted in a reduction in crown weight. Field trials

revealed that mesotrione can be phytotoxic to asparagus and could result in decreased yields (Rodriguez-Sal-amanca, 2010). Future research should investigate the e) ect that certain management regimes (including herbi-cides) have on asparagus plant vigor and the progression of FCRR. Overall, an e) ective strategy for combating FCRR should include a multipronged approach that includes fungicides, continuing selection for resistance against Fusarium spp., and certain cultural techniques such as avoiding herbicides that are phytotoxic to asparagus and irrigation to avoid environmental stress in asparagus.

Controlling Asparagus Miner PopulationsThe asparagus miner remains an understudied species, especially considering its role as a putative vector in the spread of FCRR in asparagus ' elds. Repeated applica-tions of the insecticide diazinon after the harvesting season reduced asparagus miner incidence and severity of FCRR, and increased yield (Damicone et al., 1987). An action threshold has not been established for timing insecticide applications that target the asparagus miner, presenting added di( culty. Although a sampling regime for the asparagus miner that uses canopy-level sticky traps has been shown to help (Tuell, 2003), sticky traps are not species speci' c, and can therefore be time-consuming to process. A sampling regime that uses fewer traps, or a trap with a species-speci' c lure, may increase the e( ciency of monitoring asparagus miner populations.

It is important to utilize IPM strategies to reduce reli-ance on insecticides and to manage populations of aspara-gus miner. One method is to incorporate biological control into a management regime for the asparagus miner, but there has only been limited research on the parasitoids of the spe-cies. In the United Kingdom, Giard (1904 c.f. Barnes, 1937) described a parasitoid, Dacnusa rondanii Giard (Hymenoptera: Braconidae), on asparagus miner. About three decades later, also in the United Kingdom, Barnes (1937) described three additional hymenopteran parasitoids of the asparagus miner: Pediobius epigonus (Walker) (Eulophidae; formerly Pleurotro-pis epigonus; Spencer, 1973), Sphegigaster sp. (Pteromalidae), and misidenti' ed Chorebus rondanii (Giard) (Braconidae) as Dacnusa bathyzona Marshall (Gri( ths, 1967). However, none of these biological control agents were evaluated for their e( cacy, nor have any parasitoids been described in the United States. This aspect of research provides potential for the future management of both the asparagus miner and the associated FCRR.

Semiochemicals are chemicals emitted from plants or insects that may be used as a tool in an IPM program to manage the asparagus miner. To our knowledge, there have been no studies on the response of the asparagus miner to the volatiles of asparagus. If compounds that are attractive to the asparagus miner are identi' ed, these could


Tab

le 1

. Ove

rvie

w o

f diff

eren

t tec

hniq

ues

used

to c

ontr

ol F

usar

ium

cro

wn

and

root

rot

(FC

RR

).

Man

agem

ent

stra

tegy

Targ

et†

Am

ount

Typ

eD

escr

iptio

nE

ffi c

acy

agai

nst

FCR

RC

hang

e in

con

diti

onC

itatio

ns

Sal

ting

NaC

lFo

a10

g L

–1 H

2OG

reen

hous

e10

0 m

L ap

plie

d 1

wk

afte

r pla

ntin

gS

igni

fi can

t red

uctio

n in

FC

RR

39%

dec

reas

e in

root

lesi

ons,

16

% in

crea

se in

root

wei

ght

Elm

er, 2

008

NaC

lFo

a1%

NaC

lG

reen

hous

eA

dded

100

mL

afte

r inf

ectio

n w

ith F

oaS

igni

fi can

t and

stro

ng

redu

ctio

n in

FC

RR

35%

dec

reas

e in

root

lesi

ons,

N

S in

crea

se in

root

wei

ght

Elm

er, 2

004

NaC

lFo

a an

d Fp

560–

1120

kg

ha–1

Com

mer

cial

fi el

dA

pplie

d th

ree

times

dur

ing

Apr

ilN

SN

SR

eid

et a

l., 2

001

NaC

lFo

a an

d Fp

1120

kg

ha–1

Res

earc

h fi e

ldA

pplie

d th

ree

times

dur

ing

Apr

ilN

o di

rect

mea

sure

of

FCR

R13

% in

crea

se in

the

no. o

f st

alks

> 0

.79

cmR

eid

et a

l., 2

001

NaC

lFo

a an

d Fp

0.32

g p

ot–1

Gre

enho

use

Cl e

quiv

alen

t to

othe

r tre

atm

ents

Sig

nifi c

ant r

educ

tion

in F

CR

R15

.3%

dec

reas

e in

root

rot,

0.55

g

mor

e fre

sh w

eigh

t per

pla

ntR

eid

et a

l., 2

001

NaC

lFo

a an

d Fp

17.1

–34.

2 m

MG

row

th c

ham

ber

Cl e

quiv

alen

t to

othe

r tre

atm

ents

Sig

nifi c

ant a

nd s

trong

re

duct

ion

in F

CR

R27

.4%

dec

reas

e in

root

lesi

ons

from

Fp,

and

33.

1% d

ecre

ase

in

root

lesi

ons

from

Foa

Rei

d et

al.,

200

1

CaC

l 2Fo

a an

d Fp

17.1

mM

Gro

wth

cha

mbe

rC

l equ

ival

ent t

o ot

her t

reat

men

tsS

igni

fi can

t and

stro

ng

redu

ctio

n in

FC

RR

14.8

% d

ecre

ase

in ro

ot le

sion

s fro

m F

p, a

nd N

S d

ecre

ase

in

root

lesi

ons

from

Foa

Rei

d et

al.,

200

1

CaC

l 2Fo

a an

d Fp

0.40

g p

ot–1

Gre

enho

use

Cl e

quiv

alen

t to

othe

r tre

atm

ents

NS

NS

Rei

d et

al.,

200

1N

H4C

lFo

a an

d Fp

34.2

mM

Gro

wth

cha

mbe

rC

l equ

ival

ent t

o ot

her t

reat

men

tsS

igni

fi can

t and

stro

ng

incr

ease

in F

CR

R11

.6%

incr

ease

in ro

ot le

sion

s fro

m F

p, a

nd 1

6.1%

incr

ease

in

root

lesi

ons

from

Foa

Rei

d et

al.,

200

1

NH

4Cl

Foa

and

Fp0.

29 g

pot

–1G

reen

hous

eC

l equ

ival

ent t

o ot

her t

reat

men

tsN

SN

SR

eid

et a

l., 2

001

MnC

l 2Fo

a an

d Fp

8.55

mM

Gro

wth

cha

mbe

rC

l equ

ival

ent t

o ot

her t

reat

men

tsN

SN

SR

eid

et a

l., 2

001

MnC

l 2Fo

a an

d Fp

0.53

g p

ot–1

Gre

enho

use

Cl e

quiv

alen

t to

othe

r tre

atm

ents

NS

NS

Rei

d et

al.,

200

1C

ultu

ral p

ract

ices

Bio

logi

cal s

oil

disi

nfes

tatio

nFr

62–1

02 t

ha–1

Aba

ndon

ed fi

eld

Gra

ss a

dded

at 8

0-cm

soi

l dep

th

and

cove

red

with

airt

ight

pla

stic

Sig

nifi c

ant a

nd

stro

ng re

duct

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et a

l., 2

006

Tab

le 1

. Con

tinue

d.


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 aspara-gus. It is not known where asparagus miner populations originate and if they use alternative hosts; it is assumed that they come from volunteer asparagus plants (N. Myers, personal communication, 2010). The types of habitats or vegetation outside production ' elds that harbor the aspar-agus miner should be identi' ed and methods pursued to suppress immigrating populations.

CONCLUSIONS AND FUTURE RESEARCHThere are >250,000 ha of asparagus globally (Benson, 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-gation of seedling nurseries, crown fungicidal soaks, and cultural strategies, including a neutral pH of the soil, no 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 miner for newly planted ' elds; (iii) identifying and increas-ing 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 making it more vulnerable); (vi) using cultural techniques to reduce natural stresses to asparagus; and (vii) delivering e) ective pesticides and fungicides via drip irrigation to the root zone. A program that results from research advances will manage asparagus miner and FCRR in a cost-e) ective manner with minimal impact on ecosystems.

AcknowledgmentsW.R.M. is funded by the C.S. Mott Predoctoral Fellowship in Sustainable Agriculture and a grant from MSUE-Project GREEEN (GR10-052).

ReferencesArmstrong, G.M., and J.K. Armstrong. 1969. Relationships of

Fusarium oxysporum formae specialis apii, asparagi, cassiae, mel-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. Loew) (Agromyzidae; Diptera). Ann. Appl. Biol. 24:574–588. doi:10.1111/j.1744-7348.1937.tb05854.x

Benson, B.L. 2009. 2009 update on the world’s asparagus

Man

agem

ent

stra

tegy

Targ

et†

Am

ount

Typ

eD

escr

iptio

nE

ffi c

acy

agai

nst

FCR

RC

hang

e in

con

diti

onC

itatio

nsA

ntib

iotic

sFa

erie

fung

inFo

a12

.49–

49.9

4 m

g L–1

(1

2.5–

50 p

pm)

Gro

wth

cha

mbe

rFr

om S

trep

tom

yces

gris

eus

Sig

nifi c

ant a

nd s

trong

re

duct

ion

in F

CR

R36

-mm

incr

ease

in a

spar

agus

sh

oot l

engt

h, 1

33%

incr

ease

in

dry

fi bro

us ro

ot w

eigh

t

Sm

ith e

t al.,

199

0

Inse

ctic

ides

Vorle

xFm

a an

d Fo

a36

3 L

ha–1

Res

earc

h fi e

ldFu

mig

ated

in fa

llN

SN

SD

amic

one

et a

l., 1

987

Dia

zino

nFm

a an

d Fo

a0.

63 k

g ha

–1R

esea

rch

fi eld

Spr

ayed

whe

n w

arra

nted

by

inse

ct a

ctiv

ityS

igni

fi can

t and

stro

ng

redu

ctio

n in

FC

RR

an

d m

ines

Dec

reas

e in

ext

erna

l and

inte

r-na

l ste

m ro

t ind

ex a

nd m

ines

fro

m O

phio

myi

a si

mpl

ex, a

nd

incr

ease

in y

ield

Dam

icon

e et

al.,

198

7

Her

bic

ides

Sim

azin

eFm

a an

d Fo

a6.

20 k

g ha

–1R

esea

rch

fi eld

Spr

ayed

beg

inni

ng o

f sea

son

NS

NS

Dam

icon

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al.,

198

7†

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its.

Tab

le 1

. Con

tinue

d.


production areas, spear utilization and production periods. California Asparagus Seed and Transplants, Inc., Davis.

Blok, W.J., and G.J. Bollen. 1996. Interactions of asparagus root tissue with soil microorganisms as a factor in early decline of aspara-gus. Plant Pathol. 45:809–822. doi:10.1111/j.1365-3059.1996.tb02890.x

Blok, W.J., and G.J. Bollen. 1997. Host speci' city and vegetative compatibility of Dutch isolates of Fusarium oxysporum f. sp. asparagi. Can. J. Bot. 75:383–393.

Blok, W.J., T.C.M. Coenen, A.J. Termorshuizen, and J.G. Lamers. 2008. The potential of biological soil disinfestation to man-age Fusarium foot and root rot in asparagus. Proceedings of the 11th International Symposium on Asparagus. Acta Hortic. 776:135–144.

Cohen, S.I., and F.D. Heald. 1941. A wilt and root rot of aspara-gus caused by Fusarium oxysporum Schlecht. Plant Dis. Rep. 25:503–509.

Counts, J.W., and M.K. Hausbeck. 2008. Strategies for managing Fusarium crown and root rot on asparagus. Proceedings of the 11th International Symposium on Asparagus. Acta Hortic. 776:167–172.

Damicone, J.P., W.J. Manning, and D.N. Ferro. 1987. In* uence of management practices on severity of stem and crown rot, inci-dence of asparagus miner, and yield of asparagus grown from transplants. Plant Dis. 71:81–84. doi:10.1094/PD-71-0081

Dan, Y. 1994. Development of Fusarium resistance of asparagus via tissue culture and gene transformation. Michigan State Univ., East Lansing.

Dan, Y., and C.T. Stephens. 1995. The development of asparagus somaclones with high levels of resistance to Fusarium oxyspo-rum f. sp. asparagi and F. proliferatum. Plant Dis. 79:923–927. doi:10.1094/PD-79-0923

Dingler, M. 1934. Die kleine Spargel* iege. Anz. Schaedlingskd. 1934:135–139.

Eichmann, R.D. 1943. Asparagus miner really not a pest. J. Econ. Entomol. 36:849–852.

Elmer, W.H. 1995. A single mating population of Gibberella fujik-oroi (Fusarium proliferatum) predominates in asparagus ' elds in Connecticut, Massachusetts, and Michigan. Mycologia 87:68–71. doi:10.2307/3760948

Elmer, W.H. 2001. Fusarium diseases of asparagus. p. 248–262 In B.A. Summerell et al. (ed.) Fusarium. APS Press, St. Paul, MN.

Elmer, W.H. 2004. Combining nonpathogenic strains of Fusarium oxysporum with sodium chloride to suppress fusarium crown rot of asparagus in replanted ' elds. Plant Pathol. 53:751–758. doi:10.1111/j.1365-3059.2004.01096.x

Elmer, W.H. 2008. Use of cultural microbiological treatments to overcome the replant problem in asparagus. Acta Hortic. 776:145–152.

Elmer, W.H., D.A. Johnson, and G.I. Mink. 1996. Epidemiology and management of the diseases causal to asparagus decline. Plant Dis. 80:117–125. doi:10.1094/PD-80-0117

Endo, R.M., and E.C. Burkholder. 1971. The association of Fusar-ium monoliforme with the crown rot complex of asparagus. Phytopathology 61:891. doi:10.1094/Phyto-61-395

Eskelsen, S., and A. Schreiber. 1997. Biologic and economic assess-ment of the impact of pesticide use on asparagus. Washington State Univ., Pullman.

Essig, E.O. 1913. Injurious and bene' cial insects of California. Dep. of Agric., California State Printing O( ce, Sacramento.

Evans, T.A., and C.T. Stephens. 1989. Increased susceptibility to Fusarium crown and root rot in virus-infected asparagus.

Physiol. Biochem. 79:253–258.Falloon, P.G., A.S. Greathead, R.J. Mullen, B.L. Benson, and

R.G. Grogan. 1991. Individual and combined e) ects of * ood-ing, Phytophthora rot, and metalaxyl on asparagus establish-ment. Plant Dis. 75:514–518. doi:10.1094/PD-75-0514

Ferro, D.N., and R.L. Gilbertson. 1982. Bionomics and population dynamics of the asparagus miner, Ophiomyia simplex (Loew), in Western Massachusetts. Environ. Entomol. 11:639–644.

Ferro, D.N., and G.J. Suchak. 1980. Assessment of visual traps for monitoring the asparagus miner, Ophiomyia simplex Agromy-zidae: Diptera. Entomol. Exp. Appl. 28:177–182.

Gilbertson, R.L., W.J. Manning, and D.N. Ferro. 1985. Associa-tion of the asparagus miner with stem rot caused in aspar-agus by Fusarium species. Phytopathology 75:1188–1191. doi:10.1094/Phyto-75-1188

Gordon, T.R., and R.D. Martyn. 1997. The evolutionary biology of Fusarium oxysporum. Annu. Rev. Phytopathol. 35:111–128. doi:10.1146/annurev.phyto.35.1.111

Graham, K.M. 1955. Seedling blight, a fusarial disease of aspara-gus. Can. J. Bot. 33:374–400. doi:10.1139/b55-033

Gri( ths, G.C.D. 1967. The Alysiinae (Hymenoptera: Braconidae) parasites of the Agromyzidae (Diptera). IV. Beitr. Entomol. 17:653–696.

Grogan, R.G., and K.A. Kimble. 1959. The association of Fusar-ium wilt and root rot with the asparagus decline and replant problem in California. Phytopathology 49:122–125.

Hartung, A.C., and C.T. Stephens. 1983. E) ects of allelopathic substances produced by asparagus on incidence and severity of asparagus decline due to Fusarium crown rot. J. Chem. Ecol. 9:1163–1174. doi:10.1007/BF00982219

Hartung, A.C., C.T. Stephens, and W.H. Elmer. 1990. Survey of Fusarium populations in Michigan’s asparagus ' elds. Acta Hortic. 271:395–401.

Hausbeck, M.K., and B.D. Cortright. 2008. New management for Fusarium and Phytophthora control in asparagus production. Great Lakes Fruit, Vegetable and Farm Market EXPO. Conf. Proc.

Hausbeck, M.K., C. Saude, and J.W. Counts. 2006. Asparagus dis-ease update. Great Lakes Fruit, Vegetable and Farm Market EXPO, Grand Rapids, MI. Conf. Proc.

He, C.Y., T. Hsiang, and D.J. Wolyn. 2002. Induction of systemic disease resistance and pathogen defence responses in Asparagus o! cinalis inoculated with nonpathogenic strains of Fusarium oxysporum. Plant Pathol. 51:225–230. doi:10.1046/j.1365-3059.2002.00682.x

He, C.Y., and D.J. Wolyn. 2005. Potential role for salicylic acid in induced resistance of asparagus roots to Fusarium oxysporum f. sp. asparagi. Plant Pathol. 54:227–232. doi:10.1111/j.1365-3059.2005.01163.x

Hodupp, R.M. 1983. Investigations of factors which contribute to asparagus decline in Michigan. Michigan State Univ., East Lansing.

Keulder, P.C. 1999. Asparagus decline and replant problem: A review of the current situation and approaches for future research. Proceedings of the 9th International Asparagus Symposium. Acta Hortic. 479:253–262.

Kna* ewski, M., Z. Fiedorow, and A. Pawlowski. 2008. Viral dis-eases and their impact on asparagus performance and yield. Proceedings of the 11th International Symposium on Aspara-gus. Acta Hortic. 776:191–198.

Lampert, E.P., D.C. Cress, and D.L. Haynes. 1984. Temporal and spatial changes in abundance of the asparagus miner, Ophio-myia simplex (Loew) (Diptera: Agromyzidae), in Michigan.


Environ. Entomol. 13:733–736.Lievens, B., M. Rep, and B.P.H.J. Thomma. 2008. Recent devel-

opments in the molecular discrimination of formae spe-ciales of Fusarium oxysporum. Pest Manag. Sci. 64:781–788. doi:10.1002/ps.1564

Mule, G., A. Susca, G. Stea, and A. Moretti. 2004. Speci' c detection of the toxigenic species Fusarium proliferatum and F. oxysporum from asparagus plants using primers based on calmodulin gene sequences. FEMS Microbiol. Lett. 230:235–240. doi:10.1016/S0378-1097(03)00926-1

Nelson, P.E., T.A. Toussoun, and W.F.O. Marasas. 1983. Fusarium species: An illustrative manual for identi' cation. Pennsylva-nia State Univ., University Park.

Nigh, J.E.L. 1990. Stress factors in* uencing Fusarium infection in asparagus. VII International Asparagus Symposium. Acta Hortic. 271:315–322.

Poll, J.T.K., and T. Huiskamp. 1992. The e) ect of the asparagus replant problem in time. Asparagus Res. Newsl. 9:18–22.

Pontaroli, A.C., and E.L. Camadro. 2001. Increasing resistance to Fusarium crown and root rot in asparagus by gametophyte selec-tion. Euphytica 122:343–350. doi:10.1023/A:1012983123410

Pontaroli, A.C., E.L. Camadro, F.J. Babinec, and A. Ridao. 2000. Responses of Asparagus o! cinalis pollen to the culture ' ltrate of Fusarium oxysporum f. sp. asparagi. Sci. Hortic. (Amsterdam) 84:349–356. doi:10.1016/S0304-4238(99)00113-2

Proctor, R.H., A.E. Desjardins, and A. Moretti. 2010. Biological and chemical complexity of Fusarium proliferatum. p. 155. In R.N. Strange and M.L. Gullino (ed.) The role of plant pathol-ogy in food safety and food security. Springer Science and Business Media, New York.

Reid, T.C., M.K. Hausbeck, and K. Kizilkaya. 2001. E) ects of sodium chloride on commercial asparagus and of alternative forms of chloride salt on Fusarium crown and root rot. Plant Dis. 85:1271–1274. doi:10.1094/PDIS.2001.85.12.1271

Reid, T.C., M.K. Hausbeck, and K. Kizilkaya. 2002. Use of fun-gicides and biological controls in the suppression of Fusarium crown and root rot of asparagus under greenhouse and growth chamber conditions. Plant Dis. 86:493–498. doi:10.1094/PDIS.2002.86.5.493

Rodriguez-Salamanca, L.M. 2010. Management of asparagus rots. Michigan State Univ., East Lansing.

Saude, C., O.P. Hurtado-Gonzales, K.H. Lamour, and M.K. Haus-beck. 2008. Occurrence and characterization of Phytophthora sp. pathogenic to asparagus (Asparagus o! cinalis) in Michigan. Phy-topathology 98:1075–1083. doi:10.1094/PHYTO-98-10-1075

Scho' eld, M. 1946. Asparagus, past and present. Food Manuf. 21:443–445.

Shoemaker, P.B. 1965. Comparative histological study of the

penetration and infection processes in seedlings of Aspara-gus o! cinalis L. and the e) ects of di) erent carbon sources on growth sporulation and acid and base production by two iso-lates of Fusarium oxysporum f. sp. asparagi. Rutgers State Univ., Newark, NJ.

Smith, A.K., and R.L. Peterson. 1983. Examination of primary roots of asparagus infected by Fusarium. Scan. Electron Microsc. 3:1475–1480.

Smith, J., A. Putnam, and M. Nair. 1990. In vitro control of Fusarium diseases of Asparagus o! cinalis L. with a Streptomyces or its polyene antibiotic, Faeriefungin. J. Agric. Food Chem. 38:1729–1733.

Snyder, W.C., and H.N. Hansen. 1940. The species concept in Fusarium. J. Bot. 27:64–67.

Snyder, W.C., and T.A. Toussoun. 1965. Current status of tax-onomy in Fusarium species and perfect stages. Phytopathology 55:833–837.

Spencer, K.A. 1973. Agromyzidae (Diptera) of economic impor-tance. Springer, The Hague.

Stephens, C.T., R.M. De Vries, and K.C. Sink. 1989. Evaluation of Asparagus species for resistance to Fusarium oxysporum f. sp. asparagi and F. moniliforme. HortScience 24:365–368.

Tuell, J.K. 2003. Fusarium and the asparagus miner (Ophiomyia sim-plex) in Michigan. Michigan State Univ., East Lansing.

Tuell, J.K., and M.K. Hausbeck. 2008. Characterization of the Ophiomyia simplex (Diptera: Agromyzidae) activity in com-mercial asparagus ' elds and its association with Fusarium crown and root rot. Proceedings of the 11th International Symposium on Asparagus. Acta Hortic. 776:203–210.

USDA. 1999. Crop pro' le for asparagus in Michigan. Available at http://www.ipmcenters.org/croppro' les/docs/Miasparagus.pdf (veri' ed 9 Apr. 2011).

Van Bakel, J.M.M., and J.A. Kerstens. 1970. Footrot in aspara-gus caused by Fusarium oxysporum f. sp. asparagi. Eur. J. Plant Pathol. 76:320–325.

Vujanovic, V., C. Hamel, E. Yergeau, and M. St-Arnaud. 2006. Biodiversity and biogeography of Fusarium species from northeastern North America asparagus ' elds based on micro-biological and molecular approaches. Microb. Ecol. 51:242–255. doi:10.1007/s00248-005-0046-x

Wong, J.Y., and P. Je) ries. 2006. Diversity of pathogenic Fusarium populations associated with asparagus roots in decline soils in Spain and the UK. Plant Pathol. 55:331–342. doi:10.1111/j.1365-3059.2006.01360.x

Yergeau, E., M. Filion, V. Vujanovic, and M. St-Arnaud. 2005. A PCR-denaturing gradient gel electrophoresis approach to assess Fusarium diversity in asparagus. J. Microbiol. Methods 60:143–154. doi:10.1016/j.mimet.2004.09.006

constraints on asparagus production: the association of ophiomyia

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