Insect Pest Management: The Lesson of Liriomyza
Michael P. Parrella and Clifford B. Keil
Abstract
The importance of serpentine leafminers in the genus Liriomyza Mik. (Diptera: Agromyzidae) has increased dramatically during the
past 5 years. Liriomyza trifotii has emerged as the dominant economic species. Reasons for the sudden prominence of L. trifotii
include: (1) misidentification of species, (2) failure of quarantine procedures, (3) lack of basic biological studies, and ( 4) an insecticide
use policy disregarding the development of insecticide resistance. The relevance of these to the general principles of insect pest
management is discussed.
L
eafminerSin the genus Liriomyza
Mik.(Diptera: Agromyzidae) have
historically been classified as
minor pests which rarely increase to eCQnomically important levels. This was due,
in part, to the associated complex of parasitic Hymenoptera. When biological control is upset, for example, through the use
of broad-spectrum pesticides (Oatman
and Kennedy 1976), leafminer populations increase above economic levels.
During the past 5 to 10 years there has
been a dramatic increase in the damage
to various ornamental and vegetable
crops caused by these leafminers. This is
exemplified by three formal conferences
(1980, 1981, and 1982) at which researchers assembled to report on the
status of research and to exchange ideas.
The goal of these industry/universitysponsored conferences was to provide
both temporary and long-term solutions
to the leafminer problem -one that had
become so serious that it has threatened
the chrysanthemum industry throughout
the United States and the celery industry
in Florida. The question of how L. trifotii
has risen to major pest status needs to be
examined. Many possible explanations are
not unique to these leafminer problems
but have broad implications to the basic
principles of insect pest management.
These include: (1) taxonomic confusion,
(2) failure of quarantine procedures, (3)
lack of basic biological-ecological studies,
and (4) use of pesticides without regard
to the development of resistance.
Taxonomic Confusion
The leafminers most often implicated in
Michael Parrella is with the Dept of
Entomology, Univ. of California at Riverside 92521. Clifford B. Keil is with the
Dept. of Entomology
and Applied
Ecology, Univ. of Delaware, Newark
19711.
22
causing economic damage in North
America are 1. sativae Blanchard and 1.
trifotii (Burgess). The former was originally described from Brazil (Blanchard
1926) and the latter from the Washington,
D.C., area (Burgess 1880). Spencer
(1973) states that L. sativae has a much
broader range, occurring in the Neotropics and Nearctic, whereas L. trifotii
was limited to the eastern half of the
Nearctic and Venezuela, until recently.
Both species occur on agricultural crops
in Florida (Spencer and Stegmaier 1973);
yet, of 40 publications dealing with Liriomyza as pests of chrysanthemum or
celery before 1981 (Parrella and Robb
1984), only four (Genung and Janes 1975,
Janes 1974a,b, 1975) specifically identify
1. trifotii. Most authors referred to 1. sativae (or its synonyms) or used Liriomyza spp. Reports in the latter category
failed to establish the relative proportions
of the species involved, or assumed that
the species are ecologically equivalent.
L. trifotii and L. sativae are polyphagous, have overlapping host ranges, and
are morphologically similar. These gen·
eral characteristics help explain the diffi·
culty encountered in making correct spe·
cies identifications and host plant associ·
ations. Spencer (1965) clarified the
proper identification of these species
through the use of adult morphological
characters. Spencer (personal communication) has indicated that these characters
normally permit reliable identification of
the two species and that it is rare for the
color characters to vary to the extent
where any doubt can arise about their
identity. Currently, the major species attacking chrysanthemum and celery is L.
trifolii (Schuster 1981, Poe 1982); 1. sativae is an insignificant pest of these
crops. Recognition that 1. trifoiii is the
dominant leafminer in these two crops
has occurred only during the past 2 years
(Schuster 1981, Poe 1982), which suggests taxonomic confusion.
An alternative hypothesis to explain the
shift in emphasis in the literature from 1.
sativae to L trifolii involves a change in
the ecological-biological relationship between the twO species. Comparative toxicity data have shown that L. trifolii is
more tolerant than L. sativae and two
other agromyzid species (Parrella and
Keil, unpublished data). Conceivably, different inherent tolerances to synthetic or·
ganic pesticides could have allowed a
more tolerant species to supplant a less
tolerant species. Price and Stanley ( 1982)
speculated that this occurred on Gypso·
phi/a, where the two species are
common. We feel that this hypothesis is
untenable with regard to 1. trifoiii and L.
sativae, primarily because pesticides have
been widely applied to celery and chrysanthemums for ca. 30 years. A shift in
species composition might be occurring
as a result of pesticide application; however, because the purported shift in dominance has occurred only in the past 2
years, misidentification of the two species
appears to have played a more important
role. Recently, Price (1982) speculated
that L. trifolii has been an important pest
of horticultural crops in Florida for over
30 years. If this is true, then misidentification of species seems likely.
The damage done to research by this
misidentification should not be underestimated. Published information on biology, parasites, insecticide efficacy, etc.,
becomes difficult to interpret because of
the taxonomic confusion. Problems with
the specific identification of Liriomyza
spp. leafminers have similarly affected the
value of published information from Arizona, California, and Texas (Spencer
1973). Recently, several publications
from South America addressing 1. sativae
as a pest of chrysanthemum have been
corrected to indicate that the species was
actually L. trifoW (Anonymous 1981).
The consequences of misidentification are
most severe in Florida. Even where
BULLETIN OF THE ESA
voucher specimens exist, it is difficult to
adequately address the possibility of a
species complex, and, more importantly,
the possibility
that there has been a
gradual shift in dominance from L. sativae
to L. trifolii. In 1973, Spencer stated (in
reference to the genus Liriomyza) "it is
hoped that a more accurate association
with the species of leafminer can be established by future workers."
Failure
of QuarantinelProcedures
In a survey of the California agromyzid
fauna in 1977-1978,
Spencer (1981)
concluded that L. trifalii did not occur
naturally in the state. It is suspected that
this species was brought into California
during the late 1970s on chrysanthemum
cuttings or celery transplants which are
shipped into the state from Florida. In addition, the spread of this miner into
Canada, Colombia, and England is attributed to importation of chrysanthemum
cuttings from Florida (Lindquist 1983).
The California Department of Food and
Agriculture, through the offices of local
county agricultural commissioners, routinely inspects all shipments marked as
plant material entering California. However, unless inspection personnel have
been trained in the recognition offeedingoviposition punctures made by adult leafminers, they could conceivably be overlooked. Once the cuttings are in the state
at their final destination, eclosion would
occur and the more conspicuous mines
would develop. The magnitude of the
problem associated with the potential establishment of L. trifolii on chrysanthemums or celery in California was not recognized. This could be due, in part, to the
confusion over proper identification of
the species causing damage in Florida.
The damage potential of L. trifolii was
recognized in England, where eradication
efforts have been undertaken
(Powell
1981). Through 1982, the California Department of Food and Agriculture provided a pest rating of "c," for only one
Liriomyza species,
L. huidobrensis
(Anonymous 1982). The "c" rating indicates this species is already established in
California and is considered a minor pest.
Despite crop losses caused by this pest,
no pest rating is given for L. trifolii.
Lack of Basic BiologicalEcological Studies
Knowledge of a pest's basic biology and
ecology is an inherent part of most pest
management programs. In addition, comparative
studies of different
species
SliMMER 1984
forming a complex would provide insights into the interactions between these
species over time, thus perhaps providing
another explanation for change in species
composition through a growing season or
over several years. Although L. trifolii was
the first agromyzid leafminer described
from North America, no basic biological
study had been completed until recently
(Charlton and Allen 1981, Leibee 1981a,
Parrella et aI. 1983, and Prieto 1982). In
addition, there has been no detailed biological analysis of the vegetable leafminer,
L sativae.This may be attributed to the
"minor" or "secondary" pest nature of
these leafminers. There have been excellent studies providing brief biological
sketches ofLiriomyza spp. (Wolfenbarger
1947, Musgrave et al. 1975, Lindquist
1981), but the data presented in these
publications lack sufficient detail for incorporation into a predictive pest management scheme. This lack of accurate biological information
can have serious
consequences. For example, the nominal
values selected for daily oviposition by L.
sativaeon celery in the simulation model
developed
by Musgrave et al. (1978)
were much less than those obtained by
Leibee (1981a) for L. trifoli~ the major
species on Florida celery today. Although
this does not reduce the value of the simulation method, it demonstrates the need
for more accurate species-specific biological information.
Use Patterns of Insecticides
without
Regard to Resistance Development
The pesticides used on serpentine leafminers on Florida vegetables have included the major classes of insecticides
(Table 1). The mean time to failure uselife of an insecticide in Florida since 1975
has been very short. Resistance development was suspected
as early as 1957
(Genung); however, no quantitative, baseline toxicological study has been done
with any Liriomyza spp. For L. trifolii to
be properly managed on celery or chrysanthemum, its ability to develop resistance must be addressed. In California, we
have developed a technique to evaluate
resistance levels of L. trifolii. Insecticides
are topically applied to adult female flies
of standard age; mortality is evaluated
after 24 h. With this technique, ca. 20-fold
resistance to permethrin has been documented (Fig. 1) for flies collected from
commercial chrysanthemum greenhouses
experiencing control failure. This may be
regarded as a conservative estimate of the
degree of resistance to permethrin
be-
cause L. trifolii is an imported species and
individuals probably were from populations under insecticide
pressure
in
Florida. No population in California can
be regarded as completely susceptible; we
collected our "susceptible" strain from a
bedding plant nursery which applies pesticides infrequently.
Most importantly,
permethrin was not used in the nursery.
However, because DDT and pyrethroids
had been applied for control of leafminers
in Florida before establishment in California (Table 1), the probability of crossresistance is high (Farnham and Sawicki
1976). The failure of quarantine to restrict the entry of this insect had the additional effect of allowing the establishment of a population predisposed to resistance
development
by previous
selection in Florida. The relatively shallow
slope of the dosage-mortality line for the
susceptible strain (Fig. 1) indicates a genetic heterogeneity that makes resistance
likely once selection takes place. The use
of permethrin by California growers could
have been anticipated to be a short-term
strategy, curtailed by resistance.
A colony of L. trifoli~ collected from
celery in southern Florida during an episode of control failure, has shown a ca.
16-fold resistance
to methamidophos
compared with the "susceptible" strain in
California. Again, this is a conservative estimate; the "susceptible" strain has been
exposed to organophosphates
recently.
The slopes of dosage-mortality lines are
similarly low (Keil and Parrella, unpublished data).
Presently, in California there is a "24c"
special local needs registration for permethrin on chrysanthemum.
California
has recently obtained a "section 18" ex-
Table 1. History of insecticide use on
spp. in vegetables in Florida
Ltrlomyza
Insecticide
Date
first
used
Nicotine sulfate
Chlordane
Toxaphene
Parathion
Diazinon
Azinphosmethyl
Dimethoate
Naled
Oxamyl
Methamidophos
Permethrin
Cyromazine
<1945
1947
1947
1948
1958
1961
1961
1961
1975
1977
1978
1983
Effective
field life
(yr)
11
5
10
3
13
13
13
2
4
2
See Leibee (1981b).
23
emption for permethrin and methamidophos for leafminer control on tomatoes
and celery, respectively (Stimman 1983).
The toxicological history of this species
makes resistance development likely in
these situations. The policy of using an
insecticide until its effectiveness is completely negated has removed most pyrethroids and organophosphates from the
list of possible control measures.
Most research and extension personnel
have numerous responsibilities, and many
tend to look toward a short-term solution
(demanded by growers and consumers,
particularly with an aesthetic value crop
such as chrysanthemums), with the hope
that there will be time to develop longerterm solutions. This attitude is changing,
and L trlfolii (among other species) may
be a significant factor in causing more individuals to take a longer view.
of certain parasites (J. Woets, personal
communication), which makes it less
amenable to biological control. On tomato in the Netherlands, parasites that
provide good control of L. bryoniae Kaltenbach have had limited success on L.
trlfolii. A colony of Opius pal/ipes from
Holland has been established in California
with L. sativae and L. huidobrensis as
hosts, whereas no parasitism of L. trlfotii
has been obtained. In addition, L. trlfolii
appears to be expanding its host range as
it moves into new areas through the importation of infested plant material (Parrella and Robb 1982, Prieto 1982). As L.
trlfolii moves to new host plants, the efficiency of the natural enemy complex
may be reduced as a result of morphological or chemical changes.
Although only limited biological studies
of L trifolii have been completed, the reproductive potential appears to be about
three times that reported for other economically important Liriomyza (Parrella
et al. 1981a). This large reproductive potential may provide the biological variability to explain development of mechanisms to encapsulate parasite eggs, rapid
evolution of pesticide resistance, and exploitation of a large range of taxonomically diverse host plants (Ayala 1966).
Once mechanisms suppressing population
growth have been overcome, population
The Rise to Major Pest Status
L trifolii is attacked by a large parasite
complex, and considerable research has
been directed toward maximizing the parasites' contribution to mortality (see
Schuster 1981). However, the confusion
over identification has limited a thorough
analysis of the interaction of L. trifolii
with natural enemies. There is evidence
that this species can encapsulate the eggs
growth can be extreme and destructive.
Finally, the ability of L. trifolii to de·
velop resistance to insecticides is in·
volved in its rise in pest status. The failure
to address this resistance phenomenon is
probably the factor that has contributed
most to the L. trifolii problem as it exists
today. As suggested by Reynolds (1962),
it is important to establish dosage-mortality data for promising insecticides before resistance develops in an economic
pest. Furthermore, Smith (1970) stated
that an important part of modern pest
control is to monitor the level of pesticide
resistance in major pests continuously.
This needs to be done for L trifolii wherever it occurs.
A Lesson for Insect Pest Management
Like insect pest management itself, entomology is a cooperative science where
the talents and specializations of many individuals are pOOled to help provide
short- and long-term answers to particular
insect problems. Not only are the solutions obtained as strong as the weakest
link, but it is also necessary to build on
earlier work. This is especially true when
considering the basic taxonomic status of
the arthropod that is the focus of research
efforts. Many economic entomologists are
not systematists-taxonomists, and they
Fig. 1. Standard dosage (log 10)-probit mortality curves for permethrin topically applied to L.
trifolii females of two strains, susceptible (APG)
and resistant (NP). Each data point represents a
mean of four replicates with 20 females per replicate; mortality was recorded after 24 h.
95
8.5
90
8.0
80
>t:
...I
'tl
5.5
70
~
I-
IE:
60
5.0
50
0
40
~
I-
4.5
30
iii
0
IE:
A.
20
4.0
10
m
::u
0
m
Z
-4
~
0
::u
-4
~
r::j
-<
3.5
5
3.0
2
.03 .04
.06 .08 .1
.2
.3
.4
.5.6
.8
1
2
3
4
5 6
8
10
20
DOSAGE (LOG10 MG/ML)
24
BULLETIN OF THE ESA
rely on this specialized group to make the
specific identifications.
With voucher
specimens as a guide, most economic entomologists should be capable of identifying these species as well as closely related insects. In addition, voucher specimens should always be kept and updated
periodically (Robinson 1975). Voucher
specimens of Liriomyza spp. from many
states are currently held at Virginia Polytechnic Institute and State University,
Blacksburg, (Poe and Montz 1981), thus
reducing the possibility of future taxonomic confusion. The problems encountered by researchers and systematists in
the proper identification
of Liriomyza
spp. are confusing in light of Spencer's
(1965) clarification of the status of 1. trifotil. However, the assumption of a species complex or, worse, the attitude that
the taxonomy made no difference, has reduced the value of past research on these
leafminers. Many of the possible reasons
for the rise of 1. trifolii to primary pest
status are obscure as a result of this mis·
identification. The attitude favoring a species complex has delayed work on basic
biology and ecology and has delayed the
research response to insecticide
resistance. The overall problem with misidentification would cause problems in the enforcement of quarantine restrictions even
if they were in existence.
Cineraria new to science. Rev.Soc. Entomol.
Argent. 126: 352-359.
Burgess, E. 1880. The clover Oscinis (Oscinis
trifoHi(Burgess) n. sp.). U.S.Dep. Agric. Rep.
1879: 200-201.
Charlton, C. A., and W. A. Allen. 1981. The
biology of Liriomyza trifolii on beans and
chrysanthemums,
pp. 42-49.
In D.].
Schuster [ed.], Proc. IFAS-Ind. Conf. BioI.
Control Liriomyza Leafminers n, LakeBuena
Vista, Fla.
Farnham, A. W., and R. M. Sawicki. 1976.
Development of resistance to pyrethroids in
insects resistant to other insecticides. Pestic.
Sci. 7: 278-282.
Genung, W. G. 1957. Some possible cases of
insect resistance to insecticides in Florida.
Proc. Fla. State Hort. Soc. 70: 148-152.
Genung, W. G., and M.J. Janes. 1975. Host
range, wild host significance, and infield
spread of Liriomyza trifo/ii' and population
buildup; and effects of its parasites in relation
to fall and winter celery (Diptera: Agromy·
zidae). Belle Glade AREC. Res. Rep. EV1975·5.
Janes, M.J. 1974a. Foam application of methomyl to sweet corn and leafy vegetables. ].
Econ. Entomol. 67: 249-250.
1974b. Insecticide evaluation for control of
leafminers on celery. Univ. Florida, Bell
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1975. Insecticide evaluation for control of
leafminers and beet armyworms on lettuce.
Ibid. Rep. EV-1975-1.
Leibee, G. I. 1981a. Development of Liriomyza trifolii (Burgess) on celery, pp. 3541. In D.]. Schuster [ed.], Proc. IFAS-Ind.
Conf. BioI. Control Liriomyza Leafminers.II.
Lake Buena Vista, Fla.
1981b. Insecticidal control of Liriomyza spp.
on vegetables, pp. 216- 220. Ibid.
Acknowledgment
This research W'.IS supported in part by SAFE
Endowment, Northern California Flower
Growers and Shippers Association, California
Association of Nurserymen, South Bay
Growers, Inc., Fla., the Western Pesticide Impact Assessment Program, and the Academic
Senate at llCR. The reviews of Vince Jones,
John Trumble, and Earl Oatman, Department of
Entomology, University of California,Riverside,
as well as those of the two anonymous reviewers, were greatly appreciated.
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Received for publication
3 August
1983; accepted 20 December 1983.
•
25